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SPRINGER BRIEFS IN
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Jürgen Engel

A Critical Survey of
Biomineralization
Control,
Mechanisms,
Functions and
Material Properties
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Jürgen Engel

A Critical Survey
of Biomineralization
Control, Mechanisms, Functions and Material
Properties

123
Jürgen Engel
Department of Biophysical Chemistry
Biozentrum University of Basel
Basel
Switzerland

ISSN 2191-530X ISSN 2191-5318 (electronic)

SpringerBriefs in Applied Sciences and Technology
ISBN 978-3-319-47710-7 ISBN 978-3-319-47711-4 (eBook)
DOI 10.1007/978-3-319-47711-4
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Acknowledgements

I am grateful to Prof. Dr. Josephine Adams, University of Bristol, UK, for critical
reading of this manuscript and for many constructive suggestions. Her many cor-
rections and comments improved the text considerably. I also thank Prof. Dr. Hans
Peter Bächinger, Shriners Hospital for Children, Portland, USA, for corrections and
comments and Dr. Ulrike Engel, Nikon Imaging Centre, University of Heidelberg,
Germany, for many discussions.

v
Contents

1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.1 What Is Biomineralization? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.2 Discovery and History . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.3 Linkage with the Extracellular Matrix. . . . . . . . . . . . . . . . . . . . . 3
1.4 Why This Book? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2 Chemistry and Minerals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.1 Biominerals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.2 How to Detect Biomineralization? . . . . . . . . . . . . . . . . . . . . . . . 6
Reference . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
3 Biominerals and Their Function in Different Organisms . . . . . . . . . 7
3.1 Calcium Carbonate Biominerals . . . . . . . . . . . . . . . . . . . . . . . . . 7
3.2 Silica Biominerals and Silia Biomineralization . . . . . . . . . . . . . . 9
3.3 Iron Oxide Biominerals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
4 Different Types of Molecular Control of Biomineralization . . . . . . . 13
4.1 Genetic Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
4.2 Transport Processes in Biomineralization . . . . . . . . . . . . . . . . . . 14
4.3 The Central Process: Mineral Formation . . . . . . . . . . . . . . . . . . . 14
Reference . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
5 Enamel is the Hardest Biomaterial Known . . . . . . . ............. 17
5.1 Formation of Enamel by Vectorial Secretion
from Ameloblasts . . . . . . . . . . . . . . . . . . . . . . . ............. 17
5.2 Biomineralization Is a Replacement of Proteins
by Mineral . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
5.3 Gene Deletions and Pathological States . . . . . . . . . . . . . . . . . . . 23
5.4 Open Questions and Speculations . . . . . . . . . . . . . . . . . . . . . . . . 23
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27

vii
viii Contents

6 Formation of Mollusk Shells . . . . . . . . . . . . . . . . . . . . . . . ......... 29

6.1 Morphology and Structures . . . . . . . . . . . . . . . . . . . . ......... 29
6.2 Role of Secretion and Organic Matrix: Many Data
and Many Questions . . . . . . . . . . . . . . . . . . . . . . . . . ......... 32
6.3 Little Genetic Overlap Between Shell Proteins . . . . . ......... 37
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ......... 40
7 The Glasshouse of Diatoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .... 41
7.1 Formation of the Siliceous Cell Wall During Cell Division .... 43
7.2 Si(OH)4 Uptake by Silicic Acid Transporters . . . . . . . . . . . .... 44
7.3 Does a Matrix of Extracellular Proteins Model
the Cell Wall?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .... 45
7.4 Exocytosis, Secretion, and the Cytoskeleton May
Determine Cell Wall Shape . . . . . . . . . . . . . . . . . . . . . . . . .... 47
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .... 48
8 In Vitro Studies of Mineral–Protein Interactions . . . . . . . . . . . . . . . 51
8.1 Solid-State NMR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
8.2 Comparison of Biogenic and Solvent-Grown Crystals . . . . . . . . 53
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
9 What Can We Learn from Biology for Material Science? . . . . . . . . 55
9.1 Materials by Biological Methods . . . . . . . . . . . . . . . . . . . . . . . . 56
9.2 Materials by Bioinspired Processes . . . . . . . . . . . . . . . . . . . . . . . 56
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
10 Biomineralization Processes for Future Research . . . . . . ......... 59
10.1 Life with Compass: Magnetotactic Bacteria . . . . . . . ......... 59
10.2 The Largest Biosilica Structure on Earth: The Deep
Sea Glass Sponge . . . . . . . . . . . . . . . . . . . . . . . . . . . ......... 60
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ......... 61
11 Outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64
Chapter 1
Introduction

1.1 What Is Biomineralization?

Some 600 million years ago, biological evolution altered the genes of mollusks in a
way that enabled them to incorporate calcium carbonate in the form of its mineral
calcite. The shells of the mollusks provided an effective protection of the delicate
soft body of the organism. The merging of organic and inorganic compounds was a
big achievement in evolution. Today, mineral incorporation is observed in many,
but not all, living organisms. About 40 different inorganic materials and many
forms of minerals are used. The minerals are usually in a microcrystalline form but
may also be amorphous or in a glass-like state. Functions of mineralizations are
manifold, but usually an improvement of mechanical strength is observed. Unique
mechanical properties were achieved, and this attracts the interest of workers in
materials science. Over geological timescales, whole mountains have been formed
by the deposition of biologically formed minerals.
The chemical nature of biominerals, the sites of deposition, the type of crystals,
and the patterns of deposition are all genetically controlled by the organism.
Processes which lack this control, such as ossification, do not fall within the field of
biomineralization.

1.2 Discovery and History

The term biomineralization was coined by Heinz Löwenstam who discovered and
studied mineralized tissues in a wide range of animals from different phyla.
Löwenstam (often called Lowenstam in English texts) was born in Germany in
1912 and died in California in 1993. He studied biology, crystallography, geology,
and paleontology in Munich. As a Jew, he was not allowed to finish his Ph.D. at
this university under the Nazi rules and emigrated to the USA in 1936. He started

© The Author(s) 2017 1

J. Engel, A Critical Survey of Biomineralization,
SpringerBriefs in Applied Sciences and Technology,
DOI 10.1007/978-3-319-47711-4_1
2 1 Introduction

his field studies in Israel and continued in Chicago. Later he was appointed full
professor at Caltech, where he developed isotope techniques together with
Harold C. Urey. He applied very many different techniques combined with a deep
interest in biological evolution and mechanisms. Long interviews with Heinz
Löwenstam were published in the Archives of the California Institute of
Technology in 1988 [1]. These are still accessible and provide a highly interesting
biography with deep insights in history of science (Fig. 1.1).
I met Heinz Löwenstein in 1963, when I was a postdoctoral fellow at the
Weizmann Institute of Science. I learned from him about snails with mineralized
teeth and other strange topics. These were completely new to me at this time.
Löwenstam impressed me as a scientist and person. Stephen Weiner, a former
student of Löwenstam, is at present director of the Department of Crystallography
at the Weizmann Institute. In 1989, Löwenstam and Weiner published a book “On
Biomineralization” [2]. This book and early reviews [3–6] opened a new field of
biology.
It was shown that mineralization occurs in very many different organisms,
ranging from bacteria, algae, mollusks, and corals to plants and mammals to mention
a few examples. In the words of evolutionary biologists, biomineralization devel-
oped in all phyla. Many different inorganic compounds are involved, and these occur
in the form of various minerals. Biominerals usually differ from the minerals found
in the inorganic environment and from the thermodynamically most stable forms.
My first touch with biomineralization happened by meeting Heinz Löwenstam.
At this time and in the following 40 years, I was working on the structure and
function of collagens and other proteins of the connective tissue (skin, cartilage,
blood vessels, and others), all of mammalian origin. Typical constituents of con-
nective tissues are very large multifunctional proteins, which are located in the
extracellular matrix (ECM). Many of the ECM proteins are intimately connected to
minerals in calcified tissues such as bone or teeth. The focus of the work of my
research group was on the side of the proteins, but I maintained an interest how
these proteins may catalyze and control mineralization. I was fascinated by the

Fig. 1.1 Heinz A.

Löwenstam in his laboratory
at the California Institute of
Technology, Pasadena, USA,
from [1]
1.2 Discovery and History 3

ability of organisms to incorporate inorganic material and to build with them

devices with sophisticated functions.
The book by Löwenstam and Weiner put forward some ideas of how an
extracellular matrix protein might interact with a mineral crystal. The dimensions of
a protein b-sheet were shown to fit the molecular distance of Ca++-ions in aragonite
and calcite. The proposed models were, however, rather hypothetical and not
connected to defined proteins. Explosive new research sheds light on this problem,
without yet giving a complete answer.

1.3 Linkage with the Extracellular Matrix

In organisms in which mineralization does not occur, the shape and mechanical
strength of their tissues is mainly determined by cell walls (in plants or fungi), or
the extracellular matrix ECM (in animals), a complex assembly of proteins and
polysaccharides. The metazoan ECM consists of highly organized assemblies, and
tissues are formed by these organic compounds by self-assembly and under the
control of cells. Typical structures of the extracellular matrix such as skin, cartilage,
and tendon in animals and ligament in plants produce high tensile strength and
elasticity but lack hardness and mechanical resistance. By biomineralization, the
hardness of the tissue is much increased. This was a big evolutionary advantage for
many organisms. For example, only by mineralization was the development of large
animals with an endoskeleton possible. Also teeth are of great evolutionary
importance. Teeth allow uptake of otherwise inaccessible foods (snails with teeth
began to eat corals) and led to critical improvements of the digestion system. This
was only possible with extremely hard and long-lasting covers such as the enamel
of vertebrates or magnetite and strontium oxide for the snails, chitons, and limpet.
In most cases, matrix components and biominerals are closely linked. For
example in bone and teeth, the matrix protein collagen type I and the crystals of
hydroxyapatite are located in close neighborhoods. In the beginning of matrix
research, it was believed that collagen or other well-known components of the
extracellular matrix direct and control biomineralization. This is only partially true.
More recent data indicate that a rather large number of later evolving and
lineage-specific proteins are involved in control of biomineralization. Many of these
proteins have been identified and many are essential for a particular biomineral-
ization process, but the details of their action are only very partially understood.
During the last 25 years, modern methods of genetic, genomics, and protein
structure elucidation have defined some candidate proteins. Also models of mineral
formation by secretion mechanisms have been developed. Gene deletion experi-
ments show that at least 3 proteins and 2 proteinases are absolutely required for the
formation of enamel. The presence of an intact basement membrane composed of
the matrix proteins laminin, collagen IV, and perlecan was also shown to be
essential for enamel formation. My own research activities centered around the
basement membrane and its component proteins [7, 8]. Furthermore, according to
4 1 Introduction

recent reports, members of the SPARC/BM-40 family are believed to be essential

for biomineralization of enamel. In 1996, we solved the atomic structure of this
protein [9], but at this time we were not sure what its exact function was. These
were the reasons why I followed the literature on biomineralization.

1.4 Why This Book?

Strangely, all basic textbooks dealing with biochemistry and cell biology com-
pletely ignore the field of biomineralization. It is no surprise that students are, in
general, unfamiliar with mineralization processes although they are of substantial
physiological importance for the organisms and of high medical importance. The
present book will fill this gap by teaching essential features and mechanisms of
biomineralization. It will not compete with specialized texts that describe the full
repertoire of the widespread mineralization processes in nature but will focus on
basic features. The first 4 chapters will give an overview. The next 3 chapters are
devoted to processes for which the details of the molecular mechanisms of min-
eralization have been elucidated. This implies the genetic control, the elucidation of
the proteins involved, and the essential actions of cells for the correct arrangements
of the mineral phases. We will see that very interesting features are known but that
many essential problems remain unanswered. The last 2 chapters deal with
non-biological studies of mineral–protein interactions and with material science.
Hopefully, the book may help to stimulate future research in this interesting and
important field.

References

1. Lowenstam H Interview by Heidi Aspaturian, June 21–August 2, 1988. http://resolver.caltech.

edu/CaltechOH:OH_Lowenstam_H
2. Lowenstam HA, Weiner S (1989) On biomineralization. Oxford Press
3. Lowenstam HA (1981) Minerals formed by organisms. Science 211(4487):1126–1131
4. Mann S (2000) The chemistry of form. Angew Chem Int Ed Engl 39(19):3392–3406
5. Bauerlein E (2003) Biomineralization of unicellular organisms: an unusual membrane
biochemistry for the production of inorganic nano- and microstructures. Angew Chem Int Ed
Engl 42(6):614–641
6. Addadi L, Weiner S (2001) Crystals, asymmetry and life. Nature 411(6839):753, 755. doi:10.
1038/35081227
7. Timpl R, Oberbaumer I, von der Mark H, Bode W, Wick G, Weber S, Engel J (1985) Structure
and biology of the globular domain of basement membrane type IV collagen. Ann N Y Acad
Sci 460:58–72
8. Beck K, Hunter I, Engel J (1990) Structure and function of laminin: anatomy of a multidomain
glycoprotein. FASEB J 4(2):148–160
9. Hohenester E, Maurer P, Hohenadl C, Timpl R, Jansonius JN, Engel J (1996) Structure of a
novel extracellular Ca(2+)-binding module in BM-40. Nat Struct Biol 3(1):67–73
Chapter 2
Chemistry and Minerals

2.1 Biominerals

Biominerals are minerals which are formed in an organism under the control of
genes; these genes encode matrix components or proteins needed for enzymatic
activity, trafficking, or other cellular activities. They often differ from the thermo-
dynamically most stable form that is found in the non-biological environment. The
formation of biominerals needs catalysis by the living organism. Often it is not
possible to prepare them in vitro.
About 40 different biominerals are known [1]. Most frequent are calcite, arag-
onite, and vaterite composed of calcium carbonate, Ca2CO3, and hydroxyapatite
[formula Ca10(PO4)6(OH)2] composed of calcium phosphate, Ca5(PO4)3OH. Opal,
the amorphous glass state of siliciumdioxide, SiO2(H2O)n, is also very frequent.
Magnetite, a mineral with the chemical composition Fe2+Fe23+04 has attracted much
interest because of its magnetic properties. Note that minerals are known that have
identical chemical composition yet with different symmetry properties. The struc-
tural properties of these minerals including the distance between their constituent
ions will be quite different. For example, the distance between Ca2+ atoms in calcite
differs from those in aragonite, a fact which is important for the potential interaction
with regulatory proteins.
Most biominerals are found in a microcrystalline state. The microcrystals have
an elongated shape or a plate-like structure. Typical dimensions are 10–100 nm.
Depending on the mineralized system, the microcrystals are arranged in a large
variety of structural assemblies. Some minerals are found in an amorphous state,
such as is opal of silica, which is formed in a solid amorphous state, often called the
glass-like state.

© The Author(s) 2017 5

J. Engel, A Critical Survey of Biomineralization,
SpringerBriefs in Applied Sciences and Technology,
DOI 10.1007/978-3-319-47711-4_2
6 2 Chemistry and Minerals

2.2 How to Detect Biomineralization?

Detection of biomineralization is often very straightforward. For example the

hardness of mollusk shells, corals, and enamel and their resistance against com-
bustion suggests an inorganic nature. In these cases, sufficient material is available
for chemical analysis, X-ray crystallography, and other methods. Although the
mineralized material may look rather uniform at a first glance, investigation by
high resolution methods such as electron microscopy will reveal patterns of
microcrystals.
In many cases, characterization of biominerals is more difficult. For small objects
like magnetite crystals in bacteria, the Mg Calcite containing chewing elements of
sea urchin or the stinging needles of nettles, a high contrast in electron microscopy
images may provide the first hint of the presence of a mineral. A technical problem
may arise with thin sections. Tissues are normally demineralized before sectioning
in order to save the quality of the precious knives. Electron dispersive X-ray
spectrometer (EDS) attachments are frequently combined with scanning and
transmission electron microscopes. With them an elemental analysis is possible, yet
the full identification of the mineral remains open. In some cases, removal of the
organic parts of the organism may be of help. A classical example is the diatoms.
Their highly sophisticated skeletons made of amorphous opal are best visible by
light and electron microscopy of diatomaceous earth, also called Kieselguhr. This
materia is composed of fossils of the algae in an organic-matter-free state.

Reference

1. Mann S (2001) Biomineralization, principles and concepts in bioinorganic materials chemistry.

Oxford University Press
Chapter 3
Biominerals and Their Function
in Different Organisms

3.1 Calcium Carbonate Biominerals

Very different forms of biomineralization have developed during evolution.

Organisms which adopted mineralization during their evolution are found in almost
all groups of living organisms, ranging from bacteria to mammals. Different min-
erals of different composition were selected because of their functional properties
but also by their availability in the habitat of the particular organism. A large
fraction of organisms adapted calcium carbonate in its different crystal forms or
amorphous states (Table 3.1).
The structural and functional aspects of biomineralization can be very different
in different systems. The last two columns of Table 3.1 indicate only global features
by a single key word. Detailed inspection of some of these organisms reveals
fascinating functional aspects. In other cases, the functions of the biomineral are
still unexplored and open to speculation. For mollusks and corals, mechanical
shielding and chemical support are the predominant features achieved by a min-
eralized exoskeleton. In many echinoderms (sea urchins, sea stars, and cucumber),
biomineralization gives rise to complex skeletons made of a material called stereo
[2]. This complex structure is composed of calcite or Mg calcite crystals percolated
by channels in which living cells proliferate. The crystals differ in shape from
geological calcite. Furthermore, geologically formed calcite breaks easily along its
crystal planes whereas sea urchin calcite breaks more like a glass, which has no
order at the atomic level. The independence of mechanical strength from direction
is a very important material property. It prevents the disturbing easy cleavage along
symmetry planes of crystals. Orientation independence is often caused by a crystal
pattern in which the microcrystals run in different directions or by occluded pro-
teins. The most impressive skeletal structures in the sea urchin are the
self-sharpening teeth in the chewing organ, named Aristotle’s lantern because of its
shape.

© The Author(s) 2017 7

J. Engel, A Critical Survey of Biomineralization,
SpringerBriefs in Applied Sciences and Technology,
DOI 10.1007/978-3-319-47711-4_3
8 3 Biominerals and Their Function in Different Organisms

Table 3.1 Calcium carbonate biominerals, modified from [1]

Mineral Organism Location Function
Calcite Trilobites Eye lens Imaging
Mollusks Shell Exoskeleton
Crustacean Cuticle Mechanical strength
Birds Egg shell Protection
Mammalian Inner ear Gravity sensor
Mg calcitea Echinoderms Skeleton Strength, protection
Aragonite Scleractinian corals Cell wall Exoskeleton
Mollusks Shell Exoskeleton
Gastropods Love dart Reproduction
Vaterite Gastropods Shell Exoskeleton
Ascidians Spicules Protection
Amorphous Plants Leaves Calcium storage
a
In Mg calcite, 50 % of calcium is replaced by magnesium

The time at which biomineralization originated in evolution can be estimated

from the fossil records. Fossilized mollusk shells composed of calcite and aragonite
have been found which are about 600 million years old. The origin of biominer-
alization in bacteria and diatoms likely occurred earlier in evolution but are more
difficult to date from fossils.
The type of mineral, its localization and the sophisticated fine structure of the
mineralization is highly controlled by biological mechanisms. Modern mollusks
need about 500 genes or proteins to control their shell formation (Chap. 6). Corals
also contain calcium carbonate spicules, mainly in the form of the mineral arago-
nite. Fossils of coral-like species date back to the Cambrian period some 460
million years ago. The abundance of coral during earth’s history is manifested by
the enormous reefs in the oceans and by the Jura mountains.
For vertebrates, hydroxyapatite [formula Ca10(PO4)6(OH)2] is the predominant
biomineral (Table 3.2). This mineral is not compositionally pure and contains often
lattice defects. For example in carbonated apatite some of the PO43− ions are
replaced by CO32−, or Ca2+ can be replaced by Mg2+ or Sr2+ at some lattice points.

Table 3.2 Calcium phosphate biominerals, modified from [1]

Mineral Organism Location Function
Hydroxyapetite Vertebrates Bone Endoskeleton
Mammals Teeth Cutting, grinding
Fish Scales Protection
Octacalcium phosphate Vertebrates and chitons Teeth Precursor phase
Bivalves Gills Ion store
Mammals Mitochondria Ion store
Mammals Milk Ion store
3.1 Calcium Carbonate Biominerals 9

Hydroxyapatite is normally found in a crystalline state whereas the related octa-

calcium phosphate mineral [formula Ca8H2(PO4)6] is found in an amorphous state.
Some authors claim that calcium phosphate biominerals offer mechanical
advantages over calcium carbonate in the formation of bone and dentine. The
endoskeleton composed of many variants of bone and related structures is of utmost
importance for mammals and other vertebrates. From a biological point of view
bone is an extremely complex and dynamic system with a balance between bone
forming and bone degrading cells. In the present survey I shall not deal with bone.
I feel that simpler biomineralization systems are more suitable for answering basic
questions about the mechanisms of mineralization.

3.2 Silica Biominerals and Silia Biomineralization

Silica-based minerals are by far the most abundant minerals on earth. It is therefor
not surprising that silicates, SiO2, have been taken up by many organisms. In the
inorganic world, insoluble minerals such as granite (CaSiO3) predominate, but
under certain conditions silicon dioxide, often called silica, dissolves in aqueous
systems under mild conditions and neutral pH to form orthosilicic acid, Si
(OH)4 = SiO2(H2O)2. This compound spontaneously polymerizes to linear silane
chains with the repeat –O–Si–O–Si–O–. At a certain degree of oligomerization the
chains precipitate and form nanoparticles.
Silica biomineralization is an important feature of many land and marine plants
[3]. Only in living organisms are complex structural organizations of silicates
formed, that range from amorphous nanoparticles to delicate microscopic skeletons
such as the glass house of diatoms (Chap. 7). The mineral forms are frequently
comparable to opal in that the silica is not crystalline but exists in an amorphous
glass-like state. Fibrillar assemblies have also been reported [4].
From phylogenetic data, it is estimated that incorporation of silica into plants
originated around 400 million years ago. Examples of land plants with silica
minerals are stinging nettles, horsetail equisetum, certain grasses, and bougainvillea
leaves. An old German name for horsetail equisetum is Zinnkraut. Zinn in German
means tin. Because of its silica content, Zinnkraut was very effective for cleaning
the tin plates of our forebears. The major biological functions of biomineralization
in plants are structural support, pathogen defense, and light conductivity. Stinging
nettles use silica for a more specific purpose, namely the delicate construction of its
stinging hairs [5] (Fig. 3.1).
For most plants, little is known so far about the molecular details of biomin-
eralization. An exception is the diatoms which have developed to an instructive
model system. In recent years, a number of important general events of biomin-
eralization have been elucidated for diatoms. These include the transmembrane
transporter proteins of silica and the identification of protein involved in the control
of the mineralizing process (Chap. 7).
10 3 Biominerals and Their Function in Different Organisms

Fig. 3.1 Light microscopic picture of hairs (trichosomes) of the common stinging nettle (Urtica
dioica). Hairs are several millimeters long and are found on leaves and stem. They start with a
bundle of cells from which the silica containing hair-like cell emerges. The content of silica
increases from bottom to top. Most interesting is the tip of the hair at which a small globe is
located. The globe is connected to the hair by a short and very thin rod, which acts as a breakage
point. The globe is filled with a mixture of histamine, acetylcholine, and 5-hydroxytryptamine or
other toxins depending on the nettle species. A very weak touch by an animal leads to breakage of
the rod and release of the toxin. The broken rod has a very sharp glass-like structure, which injures
the skin of the animal and opens it for penetration of the toxin

3.3 Iron Oxide Biominerals

Several iron oxide minerals are known, of which magnetite is of particular interest
because of its unusual function. Magnetite is composed of iron oxide, Fe304, of
mixed valence (FeIII2FeIIO4). In a crystalline state, it shows magnetic properties
and linear chains of crystals serve as a compass needle. The biomineral is also very
3.3 Iron Oxide Biominerals 11

Table 3.3 Iron oxide Mineral Organism Location Function

biominerals, modified
from [1] Magnetite Bacteria Intracellular Magnetotaxis
Chitons/limpet Teeth Grinding
Tuna/salmon Head Magnetic
navigation

hard and provides the cutting face of the teeth of limpets and chiton. The teeth are
arranged in a tongue-like organ called the radula (Table 3.3).
Only a selection of biominerals and their function are discussed in the present
chapter. The survey, however, clearly demonstrates the large number, complexity,
and diversity of biomineralization processes. Most of these have been studied only
at a descriptive level, mainly based on morphology. Only a smaller number of
studies have dealt with the molecular details of biomineralization processes and
their control [4]. This research is only at its beginning, and many essential questions
are still open. In the following chapters, I shall focus on three well-investigated
systems, namely enamel formation in mammals, shell formation of mollusks, and
formation of the glass-like cell wall of diatoms.

References

1. Mann S (2001) Biomineralization, principles and concepts in bioinorganic materials chemistry.

Oxford University Press, Oxford
2. Addadi L, Weiner S (2014) Biomineralization: mineral formation by organisms. IOP
Publishing Royal Swedish Academy of Science. Phys Scr 098003 (13 pp)
3. Trembath-Reichert E, Wilson JP, McGlynn SE, Fischer WW (2015) Four hundred million
years of silica biomineralization in land plants. Proc Natl Acad Sci USA 112(17):5449–5454
4. Perry CC (2009) An overview of silica in biology: its chemistry and recent technological
advances. Prog Mol Subcell Biol 47:295–313
5. Thurston EL (1974) Morphology, fine structure, and ontogeny of the stinging emergence of
urtica dioica. Am J Bot 61(8):809–817
Chapter 4
Different Types of Molecular Control
of Biomineralization

The aim of this chapter was to show the complexity of mineralization processes in a
global way. It may serve as an introduction to Chaps. 5, 6 and 7 in which detailed
results in three fields of mineralization research are given. I feel that a general
introduction may be useful for non-biologists.

4.1 Genetic Control

The proof that biomineralization is under genetic control follows directly from the
identity of the mineralization pattern of parents and offspring. The glass house of a
diatom mother is identical to the glass house of the daughters (see Chap. 7). Also,
young mollusks have the same beautiful shells as their ancestors (Chap. 6). Genetic
diseases in organisms may produce alterations of mineralization. Missing genes
may lead to large disturbances in enamel formation (Chap. 5).
Gene deletion experiments, predominantly carried out with mice, have shown
that a large number of specific proteins are needed for biomineralization. In the case
of enamel formation (see Chap. 5), knockouts of genes encoding three proteins and
two matrix proteases each led to severe retardation of enamel formation. A related
genetic disease is called amelogenesis imperfect (AI). Interestingly, the enamel
layer disappears when basement membrane assembly is blocked by mutations in
one or other basement membrane constituents. This finding provided the first clear
evidence for an important role of basement membranes in enamel formation. All
epithelial layers, for example, in tissues, such as skin and blood vessels, are
underlined by a basement membrane. Basement membranes are protein layers
composed of the ubiquitous ECM components such as laminin, collagen type IV,
and perlecan. This common repertoire is supplemented by additional proteins’
characteristic of specialized basement membranes. The basement membrane also
orients specialized epithelial cells, the enamel-forming ameloblasts (see Chap. 5).

© The Author(s) 2017 13

J. Engel, A Critical Survey of Biomineralization,
SpringerBriefs in Applied Sciences and Technology,
DOI 10.1007/978-3-319-47711-4_4
14 4 Different Types of Molecular Control of Biomineralization

Gene deletion experiments and genetic diseases define the essential proteins but do
not answer the mechanistic questions about in which of the many steps of
biomineralization these proteins play a role.

4.2 Transport Processes in Biomineralization

Biomineralization may involve very many steps, of which the first are connected
with transport. The inorganic material must be taken up in a soluble ionic form by
the organism from the external environment. In plants, this may happen through the
roots and in animals by the take-up of nutrients. Marine organisms may absorb the
ions from the surrounding water. A number of transmembrane ion transporters have
been identified to be active in biomineralization. For example, a member of the
aquaporin protein family, nodulin-26-like intrinsic protein (NIP), is essential in the
transport of silicic acid into plants [1]. Membrane-bound silicic acid transporters
with 10 membrane-spanning domains pump silicic acid into the silica deposition
vesicles of diatoms (Chap. 7). This transport consumes energy and leads to high
concentrations.
In most cases, uptake is followed by transport of the ions to the site at which
actual mineralization process will take place. During transport, the organism has to
take care that no unwanted mineralization takes place. Mineralization inhibitors act
to keep the concentrations of the ions below the solubility product in order to avoid
precipitation. In animals, this can be achieved by binding proteins in the plasma or
bloodstream. A reversible exchange of soluble and mineralized calcium is well
known in the chicken, as egg shells dissolve when there are low Ca2+ levels in the
organism. Even at the transport level, chemical selectivity is high. This specificity
becomes even higher in the later steps of mineralization. As a result, biominerals
usually consist of a single cation and anion with few impurities.

4.3 The Central Process: Mineral Formation

The central processes of biomineralization are the deposition of mineral, usually in

microcrystalline form but also in amorphous states. The ability to form highly
ordered, chemically pure, and site-specific arrays of inorganic microcrystals is a
unique feature with little resemblance to other processes in the organisms.
Therefore, a large number of new tools have been developed at the genetic level.
Many steps can be distinguished in the complex machinery of the central process.
In Chaps. 5–7, I shall review three important biomineralization processes, which
have been studied in considerable molecular detail, namely enamel formation in
teeth, shell formation of mollusks, and the formation of the silica skeleton of
diatoms. In all three cases, some control proteins have been found and details about
the genetic regulation have been elucidated. Interesting mechanisms have been
4.3 The Central Process: Mineral Formation 15

proposed which include transport processes and orientation of microcrystals to

complex arrays by vectorial secretion. For the building of the glass house of dia-
toms, a regulated mechanism of exocytosis has been proposed. The cellular events
of regulated secretion and exocytosis appear to be a common mechanism. However,
surprisingly few similarities have been found concerning the proteins involved in
control of biomineralization. Even for closely related processes, different protein
players have been detected.

Reference

1. Trembath-Reichert E, Wilson JP, McGlynn SE, Fischer WW (2015) Four hundred million
years of silica biomineralization in land plants. Proc Natl Acad Sci USA 112(17):5449–5454
Chapter 5
Enamel is the Hardest Biomaterial Known

Enamel is the protective cover of the teeth of vertebrates [1, 2]. The mature enamel
is the most durable material in the organism and withstands high forces and the
wear of chewing and cutting for a full life span. In fossils of vertebrates, the enamel
is usually the best-preserved material.
Enamel forms while the developing teeth are still located under the skin. Tooth
formation starts in the embryo. In humans, the baby teeth are initiated in the second
month of prenatal development and the permanent teeth after about 5 months. The
formation of enamel lasts about 1 year and occurs only once. Repair processes are
discussed, but they do not follow the complex pathway of initial enamel formation.
The lack of remodeling of enamel prevents the growth of teeth during aging. Nature
has solved this problem by the evolution of several teeth of different size, which are
replaced during aging. In human, only two types of teeth are produced: baby teeth
and permanent teeth. These are replaced against each other in childhood. The
enamel cover prevents the growth of teeth, which may be needed for the com-
pensation of wear. However, growth of teeth is found in some rodents whose teeth
experience an unusually high wear due to gnawing. Their teeth have enamel only at
the front and exposed dentin on the inside. Teeth of this type elongate by synthesis
of dentine and both enamel layers in the part of the teeth, which did not yet
penetrate the flesh.

5.1 Formation of Enamel by Vectorial Secretion

from Ameloblasts

The enamel is laid down by specialized epithelial cells called ameloblast in a

sequential mechanism, which lasts up to a year in the human (Fig. 5.1). In the first
step, the basement membrane and the attached ameloblast cell layer bind to a
bone-like tissue called dentin, which will later form the inner part of the teeth.

© The Author(s) 2017 17

J. Engel, A Critical Survey of Biomineralization,
SpringerBriefs in Applied Sciences and Technology,
DOI 10.1007/978-3-319-47711-4_5
18 5 Enamel is the Hardest Biomaterial Known

Fig. 5.1 Schematic view of the time course of formation of the enamel layer of murine teeth.
Specialized epithelial cells called ameloblasts are layered on a basement membrane. At this
presecretory stage (1, 2), they recognize the dentin surface as a target for enamel formation. The
ameloblasts then protrude and partially digest the basement membrane (3) followed by the
development of secretory organelles termed Tomes’ process. (4). In the scheme, Tomes’ processes
are symbolized by arrowheads. At stage 4, the enamel-specific rods are formed. Each rod is
composed of many thousands of hydroxyapatite crystals and is formed by a single Tomes’ process
belonging to a single ameloblast cell (see Fig. 5.2). The orientations of the rods and their
interwoven arrangement are seen in electron micrographs in Fig. 5.3. Ameloblasts secrete the
inorganic material and also several proteins (see text). In the early secretion phase, the enamel is
soft and rich in the proteins: amelogenin, ameloblastin, enamelin, and others (see Table 3.1). In the
mature phase (phases 5–7), several proteinases (matrix metalloproteinase 20 and kallikrein-4-
related peptidase 4) are secreted. These digest the proteins, and the fragments are removed. In the
final phase, the mature enamel contains almost no protein and reaches its final hardness. The
timing of the entire process (phases 1–7) ranges from several months to a year. Figure modified
from [2]

Dentin is formed by different cells (odontoblasts), which are of mesenchymal ori-

gin. The coordinated formation of dentin and enamel is a striking example of a
mesenchymal–epithelial interaction in morphogenesis.
The first step of enamel formation is mediated by a basement membrane (phases
1 and 2 in Fig. 5.1) [2]. Basement membranes are layers of extracellular proteins
which play important roles in the morphogenesis of skin, blood vessels, and other
epithelial tissues. Most, if not all, epithelial cell layers are attached by integrins and
other receptors to basement membranes. The protein membranes contain collagen
IV, laminins, and perlecan as ubiquitous components. Collagen IV does not
assemble in fibrils as most collagens do; instead, it assembles into planar networks
which are believed to form the scaffold of basement membranes. Laminins are a
family of very large, cruciform, multidomain proteins of great functional variability.
Laminin molecules are trimers of three genetically different chains (a, b, and c), and
combinations of different a, b, and c chains lead to 16 different laminins in
mammals. Perlecan is also a very large and versatile protein with three gly-
cosaminoglycan chains. In addition, other proteins may incorporate into basement
5.1 Formation of Enamel by Vectorial Secretion from Ameloblasts 19

membranes and provide specialized functions. A decisive indication that the

ameloblast basement membrane is of crucial importance for enamel formation
comes from observations made from patients who suffer from diseases in which the
basement membrane is defective, as a result of mutations in laminin or other
components. Examples are epidermolysis bullosa and other skin-blistering diseases
[3]. These diseases are almost always connected with enamel disorders or a com-
plete lack of enamel formation [4]. By gene deletion of the a3 chain of laminin 5
(a3, b3, c2), laminin 6, and laminin 7, a lethal blistering condition of the skin was
induced in mice. The mutated mice also suffered from strong irregularity of enamel
formation. Defective basement membranes coupled with defective enamel are also
caused by the mutations of collagen IV, perlecan, or receptors for basement
membrane components, such as certain integrins or collagen XVII.
In phases 3 and 4 of the scheme in Fig. 5.1, the ameloblasts start to secrete via
morphologically distinct secretion organelles, called Tomes’ processes [5–7].
Initially, the so-called soft enamel is formed which has little mineral and high
protein content. This is followed by mature hard enamel which has almost no
protein. A characteristic microcrystalline structure of hydroxyapatite is formed
which is called the prismatic enamel rod. These rods are about 4 lm thick and
consist of many thousand calcium hydroxyapatite crystals. They start to grow at the
dentin surface and approach a length of up to 2.5 mm for human teeth. In the
schematic presentation of Fig. 5.2, three parallel rods emerge from the Tomes’
processes of three neighboring ameloblast cells with an orientation perpendicular to
the dentin/enamel interphase. This orientation is only observed for the first segment
near this junction at which enamel formation begins. In the enamel of the teeth of
mice, this initial segment is about 250 nm long (Fig. 5.3 left).
Across the entire span of the enamel layer, a much more complicated picture is
observed (Fig. 5.3 left). Rods emerge in at least two directions and are interwoven.
The different orientations and the interweaving are apparently the result of a
dynamic vectorial secretion in different directions by the Tomes’ processes [7]. The
growth of enamel rods starts at the dentin–enamel junction and builds up the full
thickness of the enamel layer, which by the end of the secretion phase is 2 mm
across. During the growth process of the rods, their orientation can change due to
changes in the direction of secretion. This is suggested by Fig. 5.3 left in which the
rods near to the dentin junction grow in parallel with the growth direction. This is
followed by the regions approximately 120 nm thick with different orientation
patterns. There are strong indications that the ameloblast and the Tomes’ process
are flexible and have capability to change the direction of secretion in a synchro-
nized way [7]. Data also indicate that a single Tomes’ process is responsible for the
secretion of a single enamel rod and stays connected to this rod during the entire
pathway of enamel formation. Therefore, the rods are always under the control of
the secretion apparatus. Interweaving may also be caused by the movements of the
secretory machines. The mesh width (the number of rods in the layer with different
orientations that must be passed before a rod changes to the other side) is high and
about 7–10 (Fig. 5.3 right). The large mesh width is consistent with the high
stiffness of enamel rods. In the teeth of different animals, the rods have similar
20 5 Enamel is the Hardest Biomaterial Known

Fig. 5.2 Prismatic enamel

rods (red cylinders) consist of
bundles of many thousand
calcium hydroxyapatite
crystals. Typically, they are
4 lm in diameter. They are
formed by secretion from the
secretory apparatus of the
Tomes’ processes [4–6] of
ameloblasts. Each ameloblast
cell produces a single enamel
rod. Tomes’ processes are
symbolized by arrows facing
the enamel rods

appearances, but large variations are observed in the mode of interweaving the
orientations of the rods. It must be kept in mind that artifacts of electron microscopy
and differences in edging may also influence the pictures of the enamel layer.
The mechanism of enamel biomineralization driven by an epithelial cell layer
located on a basement membrane and vectorial cell secretion is quite different from
earlier views in which inhibitors and promotors of ion binding were thought to play
the governing role. Simmers et al. [8] called it “a postclassical theory of enamel
formation.”
5.2 Biomineralization Is a Replacement of Proteins by Mineral 21

Fig. 5.3 Scanning electron micrograph of fully mineralized mouse incisor tooth enamel at low
magnification (left) and high magnification (right). The left part shows a total section of the enamel
layer of about 1.5 mm thickness and the left part a section of about 16  16 lm. Original figures
from [9]

5.2 Biomineralization Is a Replacement of Proteins

by Mineral

As already mentioned, a number of proteins are secreted before or together with the
hydroxyapatite of enamel. Amelogenin is the most abundant protein that is secreted
in the early phase of soft enamel formation. A second protein, ameloblastin, is also
rather abundant (Fig. 5.4). It is believed that ameloblastin and amelogenin form
some kind of matrix [9] which directs or helps in mineral formation. In transmission
electron micrographs of soft enamel, regions of low contrast in the electron
micrographs have been interpreted as a protein matrix. Amelobastin is believed to
cover the surface of enamel rods. According to in vitro studies with recombinantly
produced amelogenin, this protein is able to self-assemble into microspheres [1, 10].
Similar in vitro assembly experiments have been performed with ameloblastin. The
relation between this rather unspecific sphere-like assembly and the amelogenin and
ameloblastin structures in the early secreted, protein-rich soft enamel is not clear.
Certainly, the issue is yet more complicated because other proteins such as enamelin
and others are also essential for the biomineralization process.
The involvement of proteases in enamel formation was a surprising discovery
[2]. Matrix metalloproteinase 20 is a multidomain enzyme of high specificity. The
main fragments of amelogenin are shown in Fig. 5.5. These fragments were
identified by biochemical analysis of enamel. In fact, no intact amelogenin was
22 5 Enamel is the Hardest Biomaterial Known

Fig. 5.4 Three proteins and two proteinases are cosecreted with Ca2+ and phosphate ions. Several
additional proteins (tuftin, thrombospondin (not shown in the table) have been identified in small
amounts. In soft enamel, the protein content is high, yet decreases to almost zero in mature enamel.
Consequently, the mineral content increases from about 30 % to near 100 % of total mass. Note
that these values are only approximate. Data from [1, 2, 11, 17]

detectible by this analysis. This raised the question whether the fragments, rather
than the native protein, may be active in enamel formation. If so, the numerous
studies carried out with recombinantly prepared intact amelogenin should be
reconsidered. Similar fragments to those shown in Fig. 5.5 were produced when
recombinant amelogenin was treated by MMP 20, demonstrating that the cleavage
during enamel formation is indeed caused by this enzyme. There are also data,
(which will not be reviewed here), that enamelin and ameloblastin are cleaved by
the proteinases listed in Fig. 5.5. The cleavage products make up 30 % of the mass
of soft nascent enamel. In the transition to hard mature enamel, they are removed
probably by reabsorption by the ameloblast cells. The final, mature enamel contains
almost no protein, and the entire process can be viewed as a replacement of protein
by mineral. As catalysts of enamel formation, the proteins promote the reaction, but
are not part of the final product. In a strict sense, a catalyst should not be modified
during the reaction, but here a proteolytic cleavage take place.

Fig. 5.5 The main cleavage products of amelogenin. The sequence of human amelogenin is
shown, and the cleavage products are indicated in green, blue, and red. The region in bold letters is
predicted to assume the conformation of a 27-nm-long polyproline II helix
5.3 Gene Deletions and Pathological States 23

5.3 Gene Deletions and Pathological States

Further insights into the importance of enamel-associated proteins come from gene
deletion experiments. A number of studies have deleted the genes of enamelin,
amelogenin, ameloblastin and the matrix proteinase MMP20 in mice. These data
are supplemented by the pathologies of various human genetic diseases caused by
missense mutations in one of these genes. The data are very voluminous, and only a
short insight will be given.
Mutations in the human amelogenin gene (AMELX) on the X-chromosome and
the enamelin gene (ENAM) were found to cause disorders with enamel male for-
mation. Diseases caused by point mutations in the human ameloblastin gene
(AMBN) have not yet been observed; however, homozygous deletion of exons 5
and 6 in AMBN results in the lack of enamel formation. The point mutations and
exon deletion data show that these three proteins are essential for proper enamel
formation. In the wild-type situation, however, these proteins are found in mature
enamel in trace amounts only, near to the detection limit (Fig. 5.4).
Very illuminating observations have been made from scanning electron micro-
graphs of the enamel-forming region of the teeth of mice with gene deletion of
either enamelin, amelogenin, or the proteinase MMP20 (Fig. 5.6, which shows the
phenotypes of mice homozygous for each gene deletion). Homozygous gene
knockouts showed much larger effects than heterozygotes. The most dramatic effect
was observed for enamelin-null mice, in which no enamel layer with its typical rods
was observed. For amelogenin-null mice, the enamel layer was thin and the rods
were not very clearly defined. For MMP20-null mice, the enamel rods had rather
random orientations near the dentin junction in the early phase of enamel formation
(phase 1 in Fig. 5.6). In the later phase, an amorphous deposition of material was
observed. This finding seems to suggest that a lack of proper proteolysis of MMP20
substrates prevents proper rod formation. Ameloblastin-null mice have similar
phenotypes to the enamelin-null mice (not shown), and it may be concluded that
ameloblastin is also essential for enamel formation.

5.4 Open Questions and Speculations

The data reviewed above show that the hydroxyapatite biomineral is ordered in a
complex pattern of rodlike structures, starts to grow from the dentin face, and is
about 2 mm thick. This pattern formation appears to be mainly controlled by a
dynamic vectorial secretion by the Tomes’ processes of the ameloblasts. Gene
deletion experiments in mice and human genetic diseases show that the basement
membrane and a number of proteins, including two proteinases, are important for
proper enamel formation. A wide open question is how, after secretion of compo-
nents, the basement membrane and its constituent proteins influence the formation of
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river. There was a bumper crop, and the price of transport is heavy.
Finally he succeeded in securing the boat in which he and his family
had come up earlier in the season. The bargain was made for sixty-
two dollars for the trip, with a bonus of two extra at the end, if we
were satisfied. There were to be four rowers, but they didn’t keep to
the agreement. They wanted to have military escort in addition,
which we declined on account of the limited deck space in which
they and the owners have to live.
The accommodation of a river-boat is small: ours consisted of
three tiny compartments, of which we took two, finding that our beds
occupied exactly half the space, with a well between them, and our
chairs and table the remainder. The cooking was done in a sort of
well in the small deck in front of us, and it was a great satisfaction to
watch the way in which it was done by Yao and his meticulous
cleanliness. There was no lack of water, so each vegetable was
washed in clean water about five or six times. I believe the correct
number of times to wash rice before cooking is ten. It was really
astonishing to see the dishes Yao prepared on the handful of
charcoal which was used to cook not only our meals but also those
of the crew.
The scenery was very wild and beautiful, and on the whole our
crew rowed well. There was an engaging little girl of three years old,
who amused us not a little with her clever manipulation of the
chopsticks, never dropping a grain of rice: she wore two silver
bangles and two rings. Each night we moored by the bank in what
was considered a safe place, for the robbers were much dreaded by
the crew. Our live stock—chickens and ducks—were tethered out to
graze. At one place they took on a couple of unarmed police,
unknown to us, but as they would have been no use whatever had
we been attacked, I ordered them to be put ashore at the next town.
The robbers had burned many villages, we were told, driving off the
cattle, killing some of the inhabitants, and looting all that was of
value to them. All the way we passed shrines dotted along the river-
bank—one hideous fat Buddha was painted on the rock—and
incense was burnt continually by the owners of the boat. The quality
of their zeal varied relatively to the danger incurred, so we had no
need to make inquiry. At the worst part of all we had to support the
courage of the crew by a pork feast, portions of which were flung into
the air and caught by wicked-looking crows, which hovered
screaming overhead. These crows are looked upon as evil spirits of
the river needing to be propitiated.
The first important town we reached in Hunan was Yuan Chowfu,
and we found there some missionaries of the China Inland Mission
who had many interesting experiences to tell of revolutionary days.
Hunan has always been a particularly anti-foreign province, and
work has progressed slowly: it is not at all surprising that the people
should be slow to understand the object of foreigners coming to
settle among them, and every one mistrusts what they do not
understand. It needs something to break down prejudice, and in this
case the something was of a tragic nature. The missionary came
home one day to find his wife lying in the veranda with a fractured
skull and brain exposed to view: she had been attacked by a
madman, who left her for dead. It was long before she was nursed
back to a certain measure of health, with speech and memory gone.
This happened two years ago, and now she is slowly regaining
strength and her lost powers, and welcomed us with exquisite
hospitality; despite having an attack of fever, she insisted on our
staying to tea and the evening meal. Mr. and Mrs. Becker have the
supreme satisfaction of finding that from the time of the accident
their work has taken on a wholly different complexion; the people
have rallied round them and look to them for support in troublous
times. With but slight medical training Mr. Becker organized Red
Cross classes, and took charge of the wounded in the mission
premises. At one time the city was threatened by revolutionaries, the
officials lost control, and for three days he took full command and
saved the situation. He received medals and a complimentary board
from the Government, acknowledging the great services he had
rendered to Yuan Chow.
No less than nine times Mr. Becker has been caught by robbers,
but has never had a single thing stolen by them, which certainly
constitutes a record. When a pistol was put to his head, he
presented a visiting card, saying, “Take this to your Chief”: it is a fine
example of “a soft answer turneth away wrath.” On recognizing who
he is, they have always released him without any injury. He told us
that recently the robber bands have been broken up, and thought we
need have no anxiety about them. We were regaled with the first
strawberries of the season from their garden, which contained a
promising supply of vegetables, and there were goats and kids in
pens. We went away loaded with good things, and deeply impressed
by the sight of these heroic workers and their colleagues.
The principal industry of the place is white wax: special ash trees
grow here on which the insects live, but every year the insects
necessary to produce the wax have to be brought from the
neighbouring province of Szechwan. “When they reach the right
stage of development they are put in paper boxes, in bamboo trays,
and carried by the swiftest runners. These men only travel by night,
as it is essential that the process of development should not proceed
too rapidly. The boxes have to be opened every day and ventilated,
and the men secure the best rooms in the inns, so that other
travellers have to suffer if they are on the road at the same time”
(Face of China, p. 183). There were also large numbers of paulownia
trees, with their lilac flowers in full bloom: they produce a vegetable
oil used for cooking and for furniture. All this district is noted for its
trees, and much wood is brought down by a tributary river from the
Panghai district, where it is cut down by the Black Miao tribe.
The next town where we halted was particularly attractive,
surrounded by red sandstone walls and grey stone battlements. We
made a complete tour on the top of the city wall, but the houses are
so high that you cannot see into any of the courtyards. At one point
there was a fine, picturesque group of trees overhanging the wall,
otherwise the houses were built very close together, like a rabbit
warren. On the battlements were a number of most comical little
guns, some carefully protected from the weather by shrines built
over them. They looked as if they might have come out of the ark,
but were only about seventy years old, some being dated.
In the market we bought wild raspberries, which had quite a good
flavour when cooked, but they were rather tart, as they were not fully
ripe. We found wild strawberries by the wayside, but were told that
some varieties are poisonous, and those we ate were quite
tasteless.
Our next halting-place was Hong Kiang, where we arrived at 8.30
a.m., and spent a pleasant day with two missionary families, one
being a doctor’s. He was rather depressed, because the town is
under the control of a military governor of irascible temper. The
doctor’s cook had recently been suffering from insanity and was
being treated in the hospital, when he was suddenly seized and
condemned to death. The doctor, on hearing of it, went instantly to
the Governor to explain matters, but he pleaded in vain, and found
the man had been shot while he was with the Governor. Executions
are continually taking place, and so badly done that frequently the
offenders linger wounded for hours after they have been shot. Often
the doctor is begged to go and help, but what can he do? On
occasion he has been allowed to go and bring them back to life! In
one case he had taken stretchers on which to bring the sufferers
back to the hospital, but they were one too few, so that he told one
man he would come back for him. The man dare not wait for his
return, and managed, despite being in a terrible condition, to drag
himself to the hospital on foot.
Mr. Hollenwenger took us up a high hill behind the city to see the
view, and it was certainly worth while, although the heat was great.
The river winds round a long strip of land, and a narrow stream
across it could easily be made navigable so as to save the junks
having to make a detour of several miles. Another big tributary joins
the river almost opposite the stream, by which quantities of wood are
brought down from the hills. The valley is full of ricefields, and we
saw men transplanting the rice with incredible rapidity from the small
field in which it is originally raised to the larger fields where it attains
maturity.
When we got back to lunch we found Dr. Witt had to go at once to
an ambulance class, which the Governor had requested him to
undertake in view of the troops being sent to fight in the struggle now
going on between North and South. In various parts of the country
we found missionaries being used by the authorities in this way. At
the time that China joined the Allies during the war they told the
German missionaries to leave the country, but exceptions were
made in the case of many like these, whose work was felt to justify
their remaining.
The next town of importance that we reached was Shen Chowfu,
where there is quite a large group of American missionaries with
hospitals, schools, etc., whom we had been asked to visit. Their
buildings stood up conspicuously at both ends of the long river-front
of the city. We were told that the hospital had been built with
indemnity money paid by the Chinese Government on account of the
murder of C.I.M. missionaries many years ago, but which the C.I.M.
declined to accept. It is a well-known fact that such money never
comes from the guilty parties, but is extorted from the people, and
consequently is always a source of ill-will. We were told by some
charming American ladies there, how bitter the feeling had been
against them, and that for years they were guarded by soldiery and
never left their houses unaccompanied by a guard. They had
spacious gardens, and the missionaries’ families lived there without
ever going into the streets. It seemed a strange kind of existence,
and brought home to us acutely the question of mission policy. There
seem to me to be two classes of American missionary ideals—
roughly speaking—one of which is responsible for some of the finest
work possible in China and which every one must heartily admire;
such work may be seen at St. John’s University, Shanghai, and in
the American Board at Peking. But there is another increasingly
large class whose faith seems to be pinned on a strange trinity—
money, organization, and Americanization. The first necessity for
them is large and showy buildings, generally apart from the busy city
life, or at least on the outskirts of the city—this may be all right in the
case of boarding-schools, but for hospitals it renders them practically
useless. I have seen groups of residential premises miles away from
the work. The welfare of the missionaries is the foremost
consideration. The means of transport are slow, so that hours must
be spent every day by the workers getting to and from their work,
and they live a life wholly apart from the Chinese. The work is highly
organized, and they have much larger staffs than our missions
provide, as they seem to have unlimited means and men.
Undoubtedly we err grievously in the opposite direction: our
missionaries have all far more work than they can perform. Added to
that, our missionaries have about one-third of the holiday that the
Americans do and less money to make the holiday a real one. Our
societies are all hard hit by the question of finance, but it would be
better to cut down our work rather than spoil its quality by insufficient
staffing and underpay.
The third point is Americanization. A large section of missionaries
so value their own culture that they believe they can do no better
than try and denationalize the Chinese, or Indians, or whatever other
nations they may be working amongst, and transform them into
Americans. In the case of China this seems to me a most disastrous
policy, and founded on serious error. The Chinese and British
characteristic of reserve which we consider a quality they consider a
defect, and believe that familiarity breeds not contempt but
friendship. The breaking down of the reserve in the Chinese
character is only too frequently a breaking down also of moral
barriers—a disintegration of character, and opposed to the genius of
the race. The Chinese student returning from the United States is
often completely spoiled by having cast off the charming old-time
manners of his own country in favour of the hail-fellow-well-met
manners of young America. He cannot be accepted into a European
or Chinese household on his return without taking what seems to
them unwarrantable liberties, while he himself is sublimely
unconscious of the effect produced. In the same way in mission
schools the students are encouraged to familiarity with their teachers
—as for instance in the case of mixed bathing in summer resorts.
The teacher and the taught are all put on the same level, and the
respect which we have been taught to consider due to age and
learning, ceases to exist. “Manners maketh man,” and the difference
in manners is one of the greatest bars to united work, which
Christians of all denominations are trying so hard to build up in China
at the present day.
To return to our brief stay at Shen Chow. It seemed an interesting
place with fine large shops, and we should like to have made closer
acquaintance with them. However, our boatman, who always wanted
to loiter where there was nothing to be seen, showed a sudden
determination that we should leave the town before sundown and
reach a certain safe spot to spend the night. As we were always
urging him to hurry, we felt obliged to give in, and reluctantly went on
board. The Standard Oil Co. is very energetic there, and has a large
advertisement, happily in Chinese characters, which are not
aggressively ugly (like our Western advertisements) all along the
river-front, the last thing we saw as we floated down stream.
Next day we shot the big rapid, and much incense and paper was
burnt to ensure our safety. Rain fell heavily in the evening, as it had
so often done during our journey. Before stopping for the night we
came to a custom-house, where our boat was thoroughly searched
for opium. It meant that at last we were come to a place where
opium was strictly forbidden, namely into the territory under General
Feng’s jurisdiction. The Customs officers, however, were most
courteous, though thorough, and I believe would have taken our
word with regard to our personal belongings, but I preferred that they
should see we were quite willing to be examined.
At midday on the morrow we reached Changteh, and walked
through wet slippery streets a long way till we came to the C.I.M.
house. Mr. and Mrs. Bannan received us most cordially and invited
us to be their guests, as Mr. Locke (who had invited us when we
were at Shanghai) had been transferred to a school five miles down
the river and was sure we should prefer to be in the city. This was
much more convenient, and we found a week only far too short to
see all the interesting things. We spent a couple of nights at the
school with Mr. and Mrs. Locke, and took part in a Christian
Endeavour meeting. This movement has proved very successful in
some parts of China, especially for training the women and girls to
take active part in evangelization. We went down the river in a
minute motor launch, which was very handy, especially as we had to
leave at an early hour to call on General Feng. I leave to another
chapter an account of him and the city, which so obviously bore his
impress when we were there. The level of Changteh is below the
river-level sometimes to the extent of fifteen feet; then the city gates
have to be sandbagged to keep the water out.
 From Changteh we went by passenger boat to Changsha, and had
two little cabins which we converted into one for the voyage. The
whole of the roof was covered with third-class passengers and their
belongings; at night they spread their bedding, and in the daytime
squatted about or wandered round the very narrow gangway outside
the cabins, a proceeding which left us in a darkened condition. Yao
managed to prepare us savoury meals in some minute nook, having
brought the necessary stores and a tiny stove on which to cook
them. The day after leaving Changteh we crossed the wonderful lake
of Tong Ting, a lake more than two thousand square miles in extent
during the summer, and non-existent in winter. This strange and
unique phenomenon is due to an overflow of the Yangtze, and in the
summer there is a regular steamship service across the lake,
connecting Changsha with Hankow, two hundred and twenty-two
miles distant, by the river Siang and a tributary of the Yangtze.
Eventually they will be connected by a railway, which is to run from
Hankow to Canton, and of which the southern part is already in
existence—and also a short section from Changsha to Chuchow;
this is only thirty-eight miles and is mainly valuable on account of its
connexion with a branch line to the Ping Siang collieries.
Changsha is an important city, the capital of Hunan. It is large and
clean, the centre of considerable trade, and one of the newest treaty
ports, opened in 1904. The variety of its exports is interesting: rice,
tea, paper, tobacco, lacquer, cotton-cloth, hemp, paulownia oil,
earthenware, timber, coal, iron and antimony. I was anxious to buy
some of the beautiful grass cloth for which it is noted, and was taken
by a friend to some of the big shops, but found them busily packing
up all their goods, in case their shops should be looted by the
approaching Southern troops. Such doings are by no means
uncommon, and all Americans and Europeans seemed to take it as
a matter of course. Arrangements were being made to receive
terrified refugees into mission premises, and the Red Cross was
extremely busy preparing for the wounded. The rumours as to the
Governor fleeing varied from hour to hour, and it soon became plain
that the city would be undefended. Our kind American hosts, Mr. and
Mrs. Lingle, were having little Red Cross flags made to put up as
signals on places of refuge, and he came in to tell us how the tailor
who was making them had just appealed to him for help: a retreating
soldier thought to make hay while the sun shone, and was taking
possession of the sewing-machine, demanding that it should be
carried away for him by the tailor’s assistant. Mr. Lingle also
prevented another sewing-machine being stolen: evidently they were
in great request.
No more striking proof could be seen of the progress of
Christianity in China than the difference of attitude shown towards
missions in time of danger and difficulty. When I first visited China a
mission station was the most dangerous place to live in; now it is the
place of safety par excellence, to which all the Chinese flock when
they are in danger. An interesting illustration of this took place last
year. In a certain district in Shensi a notorious band of robbers came
to a Baptist Missionary and a Roman Catholic priest, and promised
to save the town where they were working if they would procure for
them six rifles. They succeeded in getting the rifles, and took them to
the brigands. When they attempted to use them, the brigands found
they had been tampered with, and decided to loot the town in
consequence. They respected, however, their promise to the men
who had brought them, evidently believing in their good faith, and
said they would spare all the Christians. The problem was how to
recognize them, for at once there were a large number who claimed
to be Christians. The robbers decided by looking at them who was
genuine and who was not. In cases of uncertainty they appealed to
the missionaries, who assure us that they had proved quite accurate
in their judgment. Christianity ought to mould the expression of a
face.
There are many missions of various nationalities at Changsha,
and all seemed extremely prosperous, most of them in large and
handsome buildings. The girls’ school, of which our hostess was the
head, stood in spacious grounds outside the city wall, and near it is
the imposing pile of the Yale mission buildings. The mission started
in 1905 when Dr. Gaze began the medical work, a hospital was
opened in 1908, and the first students graduated in 1912: it is
essentially a medical school, and differs from others as regards the
staff in having short course men sent out from Yale University as
volunteers. They are not necessarily missionaries. There are fine
laboratories for research work, a large new building for science
students, splendid up-to-date equipment in all branches of medical
and surgical work, schools for male and female nurses, beautiful
houses for the large staff of professors, library, a really beautiful
chapel, lecture rooms, dormitories, playing grounds, tennis courts; in
fact everything that can be desired on the most lavish scale, the
greatest conceivable contrast to every other mission I have seen in
China. There is a special ward for Europeans. The new Rockefeller
hospital in Peking is to outshine it in beauty, I believe, but will find it
difficult to equal it in all-round equipment, and of course will lack the
acreage, which makes many things possible in Changsha which are
impossible in Peking. “The Hunan Provincial Government has met all
the local expenses of the College of Medicine and the Hospital for
the last six years.” The Rockefeller Foundation has provided funds
for salaries of additional medical staff, and Yale Foreign Missionary
Society academic teachers and a few of the medical staff. The fees
of the patients cover about half the running expenses of the hospital.
“The campus of Yale in China in the north suburb is on rising ground
between the railroad and the river, where its buildings are
conspicuous to travellers arriving by either train or steamer” (see
Yale College in China). The only drawback seems to be lack of
patients.
One of the finest pieces of mission work I saw was Dr. Keller’s
Bible School, which is supported by a Society in Los Angeles: it is for
the training of Chinese evangelists for all missionary societies, and
they divide the time of training between study and practical work.
They looked a fine body of men, and have been greatly appreciated
by the missionaries for whom they have worked. Application for their
help is made to the school, and they do not go unasked into any
district occupied by a society. When asked to conduct a mission, a
band of men is sent, and their modus operandi is as follows: they
make a map of the district, taking an area of about three square
miles—and after a day spent in prayer the men visit systematically
every house in that area and try to get on friendly terms with old and
young, giving them some portion of Scripture and inviting them to an
evening meeting. As soon as the people have become interested,
evening classes are started respectively for men, women, boys and
girls. The children are taught to sing, as they very quickly learn
hymns and like to practise the new art both early and late. The
special feature of their work is that they go as Friends to the people,
and as their own race; and it is to Chinese only that many Chinese
will listen. The character of many a village has been changed, the
missionaries say, by these national messengers, where they
themselves have been utterly unable to get a hearing. This is an
important feature of present-day missionary enterprise, and is the
link between the Past Phase of foreign evangelization and the Future
Phase of home Chinese mission work. Changsha is full of foreign
workers of many nationalities, but mainly American.
Dr. Keller’s work has been greatly strengthened in the eyes of the
Chinese by the noble example of his mother, whose spirit has
impressed them far more than any words could have done. When
her son was home for his last furlough, he felt that he could not leave
her alone, an old lady of eighty, recently widowed, and he decided to
give up his mission work for the time being. She would not agree to
this, but decided to go out with him and make her home in China for
the remainder of her life. Who can gauge the sacrifice of giving up
home and friends at such a time of life and going to an unknown land
where men spoke an unknown tongue? She had to undergo very
great hardships at first, and now after four years the solitude presses
heavily on her. At first she was able to read a great deal and lived in
her books; but she told us that now her sight is failing the time
seems very long.
We visited a Danish mission of some size, Norwegian Y.M.C.A.
workers, and a Russian lady in charge of a little blind school. She
had had no word from home for the last two years, but was pluckily
sticking to her task. The London Missionary Society has withdrawn
from work in Hunan, but the Wesleyan Mission has a high reputation
under the charge of Dr. Warren. He is one of the men who takes a
special interest in the political side of Chinese life, and gave me
much valuable information about the different parties. Just now the
changes going on are so rapid that anything one put down would be
out of date before it could be printed. The secret forces at work
keeping up hostility between North and South were everywhere
attributed to Japanese militarism: but it is only too obvious that the
present Government is not strong or patriotic enough to deal with the
situation. It is hard enough to carry on good government in so small
and stable a country as our own, so need we wonder at the inability
to transform the whole political and social system of the vastest
country in the world.
Meanwhile the civil war is a very curious one, and happily does not
cause the bloodshed one would expect, considering the forces
engaged. We had some talk with our British Consul about the
dangers of the road, as we wanted to go south to visit the sacred
mountain of Hengshan and thence to cross fine mountain passes
into the neighbouring province of Kwangshi. Mr. Giles told us that it
would be hopeless to attempt it, as an English steamer had been
fired on the day before in the very direction we must take. The
Northern and Southern troops were in active fighting, and every day
they were coming nearer to Changsha. The Governor would
probably desert the city when the Southern army had driven back the
Northern, and no one could say what would happen! After so
discouraging a report it may seem strange that Mr. Giles said there
was to be a reception at the Consulate next day, in honour of the
King’s birthday, to which he invited us.
War seemed infinitely remote from the charming gathering, where
all the foreign community met in the sunny garden on the river-bank.
English hospitality is very delightful so far away from home, and the
cordial spirit of the host and hostess lent a special attractiveness to
the occasion. I was particularly pleased to meet a Chinese friend
there, Miss Tseng, who invited us to visit her school next day. In
Chapter VIII I have tried to give an account of this famous scion of a
famous race.
With all the educational and religious and philanthropic institutions
to be visited, it was most difficult to find time to see the monuments
of the past, but we determined not to miss the beautiful golden-
roofed temple, dedicated to Chia Yi, a great statesman of the second
century B.C. It is now transformed into a school, and we saw the
boys drilling; but they seemed an insignificant handful in those noble
courtyards, and there were no signs of proper or even necessary
equipment.
Our time at Changsha was all too short, and it ended very
pleasantly with an evening spent at the Consulate. By this time many
of the Chinese were in full flight, because of the coming Southerners,
and the city was supposed to be set on fire by incendiaries at 8 p.m.
Our steamer had retired into the middle of the river, because of the
rush of passengers clamouring to be taken on board, and the captain
was unable therefore to fulfil his engagement to dine at the
Consulate. We were promised a fine sight of the blazing city—only
happily the show did not come off—from the Consulate garden
across the river. We stayed there in the delicious summer air till it
was time to go on board, and found it difficult not to step on the
slumbering people who covered the deck when we reached the
steamer. At midnight we slipped down stream, following in the wake
of the departing Governor. The Southern troops came in a few days
later, but without the looting and fighting which has so often
happened in similar circumstances.
 Chapter VII
Present-Day Ironsides—General Feng Yu Hsiang

“There shall never be one lost good! What was shall live
as before;
The evil is null, is nought, is silence implying sound;
What was good shall be good, with, for evil, so much good
more;
On the earth the broken arcs; in the heaven the perfect
round.

All we have willed or hoped or dreamed of good shall

exist;
Not its semblance, but itself; no beauty, nor good, nor
power
Whose voice has gone forth, but each survives for the
melodist
When eternity affirms the conception of an hour.
The high that proved too high, the heroic for earth too
hard,
The passion that left the ground to lose itself in the sky,
Are music sent up to God by the lover and the bard;
Enough that He heard it once: we shall hear it by and
by.”

—Browning.

Chapter VII
Present-Day Ironsides—General Feng Yu Hsiang
 China is a land full of
surprises, and at the
present day there is an
amazing variety of
individual efforts for the
regeneration of the country
by her patriotic sons and
daughters. In some ways
the chaotic political state of
China makes these
individual efforts possible
where perhaps a more
settled government would
not admit of them. For
instance, each province is
governed by a military or
civil governor, or both; and
within a province may be
found large territories
practically controlled by
some autocratic military
official, the presence of
whose army is the potent
INN LAMP. warrant for his wishes
being executed. In the
province of Hunan, roughly
speaking in the centre of China proper, is such an area, of which
Changteh is the army headquarters.
Having travelled for many weeks through districts infested with
robbers, where law and order are mainly conspicuous by their
absence, where the land is one great poppy garden for the opium
trade, it came as a shock of surprise and delight to enter a district
where we found the exact reverse of these things.
In 1918 there was fighting between the forces of the North and of
the South throughout this district, and as the Northern forces were
defeated and the City of Changteh captured by the Southerners,
General Feng was sent from the neighbouring province of Szechuan
to re-take the city. He had not only defeated the Southern Army
there, but had treated them in an entirely new way. Feng disbanded
the Southern troops after disarming them, and presented each
officer with ten dollars and each private with five dollars, so that they
might be able to return to their homes without resorting to pillage, the
source of so much sorrow in China. The General led his troops to
Changteh and found that the Southern forces had withdrawn, so that
he entered the city unopposed, though by no means with the
goodwill of the inhabitants. They were only too familiar with the
tyranny of ordinary Chinese troops; for it is not by foreigners only
that they are evilly spoken of, but by all Chinese.
In the two years which had elapsed since then this attitude was
completely changed, for the army was paid regularly and not obliged
to prey upon the habitants for sustenance, the strictest discipline was
observed, and no soldier was allowed to loaf about the streets. The
city itself underwent a wonderful purification: gambling dens, opium-
smoking halls, houses of ill repute were swept away, and theatres
transformed into schools; now a woman even can walk the streets
day or night without fear. A notice of three days to quit was given to
the above-mentioned houses, and the order was no dead letter.
Severe fines were inflicted on traffickers in opium. The streets of the
town became wonderfully clean in another sense of the word; the
General is so particular about this that if any of the army mules or
horses pass through it they are followed by scavengers in order that
no traces of their passage may remain; for as there is no wheeled
traffic and the streets are extremely narrow there are no side-walks.
There are notices in the centre of the streets with regard to the rule
of the road, but this is too recent an innovation to be quite
understood as yet. Everywhere one is confronted with signs of the
General’s determination to raise the moral of the people. When he
closed the opium dens he opened refuges for the cure of the smoker,
instead of putting him in prison, as is done in certain parts of the
North. The patient was photographed on entering and on leaving (à
la Barnardo). General Feng punishes with death the soldier proved
to have been trafficking in the sale of opium, while the civilian is
punished by being flogged and paraded bare-backed afterwards
through the streets, preceded by a notice board stating his offence.
The city gaol is the only one in the country which has a chapel and
the missionary bodies in the town have charge—a month at a time
by turns. As you pass along the streets your eye is attracted by
posters of a novel kind. They are pictures descriptive of evil habits to
be shunned: a cock is vainly sounding the réveillé to which the
sluggard pays no heed; the vain woman on her little bound feet
watches from afar the industrious woman doing her task in cheerful
comfort with normal feet, and so on. In odious contrast to these
pictures are the British and American cigarette posters to be found
all over the country, and I was told that one of the leading
Englishmen in the trade said regretfully that he thought they had
done the country no good turn in introducing cigarettes to China.
They are considered a curse by thoughtful Chinese, and at the
request of the officers, the General has prohibited the use of them in
the army, though there is no embargo on other tobacco-smoking.

A Man of Mark.

Page 158
 Another noticeable feature of the city is the open-air evening
school, the sign of which is a blackboard on a wall, sheltered by a
little roof which may be seen in many an open space. When the
day’s work is over benches are produced from a neighbouring house
and school begins. The General has established over forty night
schools dotted along the five miles of the city on the river-bank,
besides the industrial schools open during the daytime. We visited
one large training school for girls and women, which he has
established and supports in order to promote industry, and to which
workers from the country districts are welcomed. They have six
months’ training and one meal a day gratis, and they are taught
weaving, stocking-making (on machines), dressmaking and tailoring,
etc., and the goods turned out find a ready market. The instructors
are all very well paid, and the work done is thoroughly good, despite
the disparaging remarks of an elderly overseer who evidently had
the conventional contempt for the Chinese woman’s intelligence.
General Feng is a firm believer in women’s education, and has
established a school for the wives of his officers, to which they come
not altogether willingly, I fear. The unwonted routine and discipline
are naturally a trial, especially to women no longer in their première
jeunesse; and despite the fact that he succeeded in persuading a
highly-trained and charming woman to come from the north to take
charge of it, there have been many difficulties to surmount. She
lunched with us one day and told us an instance of this which makes
one realize the situation: a certain lady resented the fact of her
teacher being the wife of a veterinary surgeon (lower in rank than her
husband), and disregarded her continual efforts to curb her feminine
loquacity and make her attend to her studies. Finally there was a
complete rupture between the ladies, and the unwilling pupil
indignantly left the school. The teacher pondered over this and could
not bear the thought of having quarrelled with a fellow Christian. She
determined to try and make it up, so she called upon the lady, who
refused to see her. Nothing daunted, she tried a second time, and
again the lady was “not at home,” but sent her husband to speak to
her. The teacher explained to him all she felt—he was so moved by
her appeal that he fetched his wife, a complete reconciliation took
place, and she returned to school.
 The General has a short religious service in his own house every
Sunday morning for these ladies, at which he, his wife and some
officers are present, and at which he invited me to speak.
Having described in outline the changes effected in Changteh by
General Feng, it is time to try and describe the man himself and his
past life. He is tall and powerful, with a resolute, masterful air as
befits a man who is ruler of men; but his ready smile and the
humorous twinkle in his eye reassures the most timid. He was born
in 1881 in the northern province of Nganhwei, of humble parentage,
and had no educational advantages. He has amply made up for this,
however, having a keen sense of the value of knowledge and giving
to others what was not given to him. The study of English is being
eagerly pursued by himself and his officers, and he will soon pick it
up if he comes to England, as he wishes to do.
General Feng entered the army as a common soldier, and in 1900
was present (on duty), but only as an onlooker, at the Boxer
massacre of missionaries at Paotingfu. This was his first contact with
Christian people, and it made a deep impression on him. This was
strengthened by further contact with a medical missionary, who
cured him of a poisoned sore and charged nothing, but told him of
the love of God, Who had sent him to heal the sick. There is no
doubt that medical missions have been one of the best possible
instruments for winning the Chinese to Christianity, and one cannot
but regret that it is now becoming necessary to abandon the practice
of non-payment, except for the most necessitous cases, on account
of the terrible rise in prices and the lack of funds for the upkeep of
our hospitals. However, it appears to be inevitable.
The turning-point in General Feng’s life took place when he was
stationed at Peking in 1911, having already risen to the rank of
Major. He was feared and disliked by officers and men on account of
his fierce temper, which caused him to strike them when he was
angry, while his wife also had to submit to being beaten when she
displeased her lord and master in the most trivial details. There was
as complete a change in his life as in Saul’s when he obeyed the
heavenly vision. This was the result of attendance at a meeting by
Dr. Mott, and he was assigned to Bishop Morris’s care for further
teaching. The strongest influence brought to bear on him at that
time, however, seems to have been that of Pastor Liu, of the
Wesleyan Mission, who became one of his best friends. It is not easy
at the age of thirty-one to conquer an ungoverned temper and
tongue, but the fact remains that he is now adored by his troops, and
that he has never abused or ill-treated his wife (a General’s
daughter) since becoming a Christian. How difficult this is may be
judged by the fact that one of the finest characters among the
Christian Chinese clergy, Pastor Hsi, says that he found it so
impossible to conquer the lifelong habit of abusive language to his
wife that he had to make it a special matter of prayer before he could
succeed, though he was such a saint. The question of bad language
throughout the army is remarkable; an American missionary, after
spending a year constantly in and out amongst the men, said he had
heard none, for the General has a wonderful way of getting his
wishes observed, and has been instrumental in winning the bulk of
both officers and men to Christianity. He has compiled a treatise on
military service, redolent of Christian morality, which every one of his
men can repeat by heart. This treatise has been taken as the basis
of General Wu Pei Fu’s handbook (a friend of General Feng), who
quotes Cromwell’s army of Ironsides as a model for the soldier’s
imitation, though he does not profess to be a Christian! It may be
thought that the Christianizing of the army is of doubtful reality, but
this is certainly not the case; for in the first place the amount of Bible
teaching they are undergoing is far beyond what would ordinarily be
the case here at home before admitting candidates to Church
membership, and the only difficulty about this teaching is to find the
teachers necessary for such numerous candidates: they are keen to
learn about Christianity. Before baptism they have to submit to a
searching examination of their character and behaviour, and must
have an officer’s certificate to that effect. In addition each man must
sign a statement promising to spend time daily in prayer and study of
the Bible, to seek the guidance of the Holy Spirit and to obey the
teaching of the New Testament.
Nevertheless, they have been baptized by hundreds, so that
already more than a third of the army (and I think the proportion must
be much greater now, as over one hundred were postponed as being