APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Nov. 2010, p. 6971–6981 Vol. 76, No.

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Copyright © 2010, American Society for Microbiology. All Rights Reserved.

MEETING REVIEW
Halophiles 2010: Life in Saline Environments䌤
Yanhe Ma,1 Erwin A. Galinski,2 William D. Grant,3 Aharon Oren,4* and Antonio Ventosa5
Institute of Microbiology, Chinese Academy of Sciences, Tianjin Institute of Industrial Biotechnology, 1 Beichen West Road,
Beijing 100101, China1; Institute of Microbiology and Biotechnology, Meckenheimer Allee 168, 53115 Bonn, Germany2;
Department of Infection, Immunity and Inflammation, University of Leicester, Maurice Shock Medical Sciences Building,
Leicester LE1 9HN, United Kingdom3; Department of Plant and Environmental Sciences, The Institute of
Life Sciences, The Hebrew University of Jerusalem, 91904 Jerusalem, Israel4; and Department of

Downloaded from http://aem.asm.org/ on April 30, 2021 by guest

Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, 41012 Seville, Spain5

The world of halophilic microorganisms is highly diverse.
Microbes adapted to life at high salt concentrations are found
in all three domains of life: Archaea, Bacteria, and Eucarya. In
some ecosystems salt-loving microorganisms live in such large
numbers that their presence can be recognized without the
need for a microscope. The brines of saltern crystallizer ponds
worldwide are colored pink-red by Archaea (Haloquadratum
and other representatives of the Halobacteriales), Bacteria
(Salinibacter), and Eucarya (Dunaliella salina).
Hypersaline environments such as saltern pond brines and
natural salt lakes present the ecologist with relatively simple
ecosystems with low diversity and high community densities. In
such systems fundamental questions of biodiversity, selection,
biogeography, and evolution in the microbial world can be
investigated much more conveniently than in the far more
complex freshwater and marine systems. The sediments of such
water bodies, however, are often inhabited by extremely di-
verse, still incompletely explored microbial communities. Dif-
ferent types of halophiles have solved the problem how to cope
with salt stress (and often with other forms of stress as well) in
different ways, so that the study of microbial life at high salt
concentrations can answer many basic questions on the adap-
tation of microorganisms to their environments. Most known
halophiles are relatively easy to grow, and genera such as
Halobacterium, Haloferax, and Haloarcula have become popu-
lar models for studies of the archaeal domain as they are much
simpler to handle than methanogenic and hyperthermophilic
Archaea. Some halophilic and halotolerant microorganisms
have found interesting biotechnological applications as well, as
shown in the last section of this report.
The 9th International Conference on Halophilic Microor-
ganisms, held from 29 June 2010 to 3 July 2010 in Beijing,
China, brought together 166 participants from 25 countries.
The 50 lectures and 112 posters presented provided an excel-
lent overview of the current state of our understanding of all
aspects of microbiology at high salt concentrations. The meet-
ing was hosted by the Institute of Microbiology, the Chinese
* Corresponding author. Mailing address: Department of Plant and
Environmental Sciences, The Institute of Life Sciences, The Hebrew
University of Jerusalem, 91904 Jerusalem, Israel. Phone: 972 2 6584951.
Fax: 972 2 6584425. E-mail: orena@cc.huji.ac.il.
䌤
Published ahead of print on 3 September 2010.
Academy of Sciences, the Chinese Society of Biotechnology,
and the Chinese Society for Microbiology. Conference chair
was Yanhe Ma. The series of symposia on halophiles started in
Rehovot, Israel, in 1978 with a meeting devoted mainly to the
properties of bacteriorhodopsin, the retinal-containing protein
of Halobacterium that was discovered just a few years earlier.
The delegates noted and applauded the presence of Janos
Lanyi in the audience, one of the attendees at the first meeting.
This initial event was followed by meetings held in 1985 (Ober-
marchtal, Germany), 1989 (Alicante, Spain), 1992 (Williams-
burg, VA), 1997 (Jerusalem, Israel), 2001 (Seville, Spain), 2004
(Ljubljana, Slovenia), and 2007 (Colchester, United King-
dom). The proceedings of the 1978, 1989, 1997, 2001, and 2004
symposia were published as books (20, 31, 56, 68, 88); selected
papers from the 1985, 2002, and 2007 symposia appeared in
dedicated special volumes of journals (FEMS Microbiology Re-
views, Experientia, and Saline Systems).
This review intends to capture emerging themes and to re-
port key interesting new findings presented at the Halophiles
2010 symposium in Beijing. The following topics were the focus
of attention and discussion.
DIVERSITY OF HALOPHILES—CULTURED
AND UNCULTURED
“Everything is everywhere: but, the environment selects”
(“Alles is overal: maar, het milieu selecteert”). This famous
quotation from Lourens Baas Becking’s 1934 book Geobiologie
of inleiding tot the milieukunde (8) can be taken as the basis for
our understanding of the distribution of halophilic microor-
ganisms worldwide. In fact, Baas Becking (1895 to 1963) had
visited many salt lakes and studied many different halophilic
microorganisms. His book and his publications from the early
1930s contain a wealth of information, largely forgotten today,
on the properties of the halophiles. Some phenomena de-
scribed by Baas Becking at the time, including the acidic nature
of the cell envelope of Dunaliella and the interrelationship of
salt requirement/tolerance and temperature in halophilic pro-
karyotes, were “rediscovered” in the 1970s, as documented by
Aharon Oren (Jerusalem, Israel) in his keynote lecture at the
opening session.
To explore to what extent in the halophilic world “every-
thing” is indeed “everywhere” and what degree of variation

6971
6972 MEETING REVIEW
may be found among different high-salt environments, micro-
bial diversity studies have been performed in a great variety of
environments. These include saltern ponds worldwide, Great
Salt Lake, the Dead Sea (16), saline lakes in Inner Mongolia
(60), African soda lakes, deep-sea brines (85), and many oth-
ers. These studies included culture-dependent approaches,
leading to the isolation and characterization of many novel
types of halophiles and new information on the abundance and
geographic distribution of the known types, as well as culture-
independent studies based on sequencing of DNA recovered
from the environment. Many posters at the meeting related to
culture-independent analyses of hypersaline environments
from around the world, including Xinjiang salt lakes; Chinese
salt mines; salterns in Goa India, Turkey, Spain, and Israel;
south Siberian hypersaline lakes; the Dead Sea; and Great Salt
Lake. Thane Papke (Storrs, CT) examined Halorubrum strains
in Spain and Algeria, and one of his conclusions was that
“migration routes are slower than mutation rates,” allowing
endemism in Halorubrum strains to develop. Shaun Heaphy
(Leicester, United Kingdom) provided a culture-independent
microbial characterization of several Inner Mongolian salt and
soda lakes and used statistical techniques to correlate the find-
ings with physico-chemical parameters of brines and geograph-
ical location. He broadly agreed that microbial populations
diverged as distance between the lakes increased, although this
was only statistically significant for the Bacteria on an inter-
continental scale (a hypersaline lake in Argentina was included
in the analysis). Factors such as pH, temperature, and Na⫹
concentration were particularly correlated with the microbial
community composition. Thus, everything may not be every-
where. More and more cases are being reported of the isola-
tion of halophilic microorganisms from low salinity environ-
ments. Thus, after almost 80 years, Baas Becking’s quotation
still inspires experiment and debate.
Application of culture-dependent methods led to the isola-
tion of a novel halophilic archaeon from seawater (at a salinity
that does not support growth of Halobacteriaceae and causes
lysis of most known representatives of the group). The prop-
erties of this new organism, to be described as a new genus and
species, Halomarina oriensis, were presented by Kentaro Inoue
(Chiba, Japan) (37). Poster presentations included a new fun-
gal isolate from a Turkish salt mine; novel haloarchaea from a
Chinese saltern, Inner Mongolian lakes, and Iranian salt lakes;
and novel bacterial isolates from Chinese salt lakes, Inner
Mongolian Lakes, Xinjiang salt lakes, Quidam Basin Quater-
nary sediments, brine wells in southwestern China, the Yellow
Sea, The South China Sea, a Korean salt flat, Iranian salt lakes,
Mexican soda environments, and salted hides. There were ad-
ditional reports on the isolation of new actinomycetes from
saline environments in China and on different bacterial halo-
philes from nonsaline sites such as soils.
HALOPHILES IN UNUSUAL ENVIRONMENTS AND
HALOPHILES EXPOSED TO MULTIPLE FORMS
OF STRESS
Most habitats explored for the presence of halophiles are
thalassohaline environments that originated by evaporation
from seawater, reflect the ionic composition of seawater, and
have a nearly neutral to slightly alkaline pH.
APPL. ENVIRON. MICROBIOL.
Deep-sea brines, found on the bottom of the Red Sea, the
Mediterranean Sea, and the Gulf of Mexico, are interesting
environments to search for novel microbes. Apart from their
increased high salinity, they are anaerobic and form character-
istically sharp brine-seawater interfaces, with some of the
brines displaying significant increases in temperature and
metal concentration. The ionic composition of the brines gen-
erally differs from that of seawater; they are anaerobic, and in
some cases the temperature can be elevated as well. The mi-
crobiology of Shaban Deep and other deep-sea brines in the
Red Sea was discussed by André Antunes (Thuwal, Saudi
Arabia). These sites, considered sterile in the past, have
yielded a number of interesting microorganisms, including
Salinisphaera shabanensis (a facultative anaerobe growing in a
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very large range of salt concentrations, from 1 to 28%) (5),
Halorhabdus tiamatea (a nonpigmented representative of the
Halobacteriales that prefers an anaerobic life style) (7), Flexi-
stipes sinusarabici (an anaerobe tolerating between 3 to 18%
NaCl) (28), and Haloplasma contractile (a contractile bacte-
rium, phylogenetically equidistant to the Firmicutes and the
Mollicutes) (6). The sites will be revisited in the near future for
further microbiological exploration.
In many athalassohaline environments, life at the ex-
tremes of high salt is combined with the need to thrive at
alkaline pH and elevated temperatures, and organisms
growing there do so at the physico-chemical boundary for
life (18). Jürgen Wiegel (Athens, GA) summarized his stud-
ies of the anaerobic halophilic, alkaliphilic, thermophilic
bacteria isolated from the Wadi an-Natrun, Egypt.
Natranaerobius thermophilus accumulates both glycine be-
taine and K⫹ for osmotic adaptation and has multiple
Na⫹/H⫹ antiporters (49) and a Na⫹-extruding ATPase,
which was characterized in-depth by Noha Mesbah (Alex-
andria, Egypt). Two new species, designated “Natranaero-
bius jonesii” and “Natranaerobius grantii” are currently being
characterized. Natranaerobius jonesii has an extremely high
requirement for chloride ions as it does not grow at less than
1.4 M Cl⫺. Other alkaline saline environments subjected to
intensive studies in recent years are the soda lakes of the
Kulunda Steppe (Altai, Russia). Dimitry Sorokin (Moscow,
Russia) summarized the wealth of information obtained
from these studies at the level of the characterization of
cultures of novel organisms, especially those participating in
the reductive part of the sulfur cycle, and from culture-
independent studies using molecular markers, as well as
measurements of the rates of microbial sulfidogenesis. In
general, sulfide production was active even in saturated soda
brines, but far more sulfide was produced in these environ-
ments from elemental sulfur and from thiosulfate than from
sulfate. Dismutation of thiosulfate and sulfite was a major
trend in soda lake isolates (78, 79).
The Dead Sea is a rare example of a low-Na⫹, high-Mg2⫹,
and high-Ca2⫹ chloride brine with a slightly acidic pH. Meta-
genomic studies are now providing information on the micro-
bial diversity in the lake, both at the time of a bloom of
microorganisms following dilution of the upper water layers by
rain floods in 1992 and during the current drying out of the
lake, causing a continuously decreasing ratio of monovalent/
divalent cations, making conditions too extreme for even the
best salt-adapted microorganisms (16).
VOL. 76, 2010
GENOMICS, EVOLUTION, AND TAXONOMY OF
HALOPHILIC ARCHAEA AND BACTERIA
Genomics of the Halobacteriaceae has come of age. Shilad-
itya DasSarma (Baltimore, MD) gave the closing keynote lec-
ture, highlighting the haloarchaeal genomes from different
genera which have been determined since the genome se-
quence of Halobacterium NRC-1 was first published (24, 53) 10
years ago. More recently completed genomes highlighted
included Haloarcula marismortui (11, 14), Natronomonas
pharaonis (26), Haloquadratum walsbyi (17), Halorubrum
lacusprofundi (http://www.ncbi.nlm.nih.gov/sites/entrez?Db
⫽genome& Cmd⫽ShowDetailView&TermToSearch⫽23834,
2009), Halomicrobium mukohataei (82), Halorhabdus utahensis
(10), Halogeometricum borinquense (46), Haloterrigena turk-
menica (73), and Haloferax volcanii (34). The list includes sig-
nificant ecological diversity, e.g., a haloalkaliphilic species, a
cold-adapted species, species adapted to life in low-Na⫹–high-
Mg2⫹ environments, and isolates showing interesting cell mor-
phologies. The sizes of these genomes range between 2.6 and
5.4 Mb. The sequencing and analysis of the genomes of Halo-
arcula hispanica and Haloferax mediterranei were announced by
Hua Xiang and colleagues (Beijing, China). DasSarma showed
that there has been an exponential increase in the sequencing
of haloarchaeal genomes over the past 10 years, and, with
next-generation sequencing methods now available, expects
that within a few years the number of published genomes of
species of Halobacteriaceae will grow even faster. Some of the
conserved properties of haloarchaeal genomes were discussed,
including the presence of large megaplasmids and minichro-
mosomes (24) and the occurrence of core acidic proteomes
(23). The data analysis also yielded the prediction of an ex-
panding haloarchaeal pan-genome with increasing numbers of
novel genes which may have applications in biotechnology.
In two presentations from the DasSarma group, additional
postgenomic work was presented. James Coker (soon to move
to Birmingham, AL) reported on studies on the expanded
TATA-binding protein and transcription factor B protein fam-
ilies of haloarchaea, showing their importance for gene expres-
sion and stress regulation (21, 77). Satyajit DasSarma (the
youngest presenter at age 13) reported on the expansion of the
HaloWeb, the haloarchaeal genome database (http://halo4
.umbi.umd.edu), which now provides access to all the public
haloarchaeal genomes and as well as a suite of tools for data
retrieval and analysis.
Environmental genomics studies increasingly show that the
genome of individual strains may be only a small fraction of the
pan-genome of the species in nature. Haloquadratum walsbyi
has become an excellent example to illustrate this, as shown by
Francisco Rodríguez-Valera (Alicante, Spain) and Mike Dyall-
Smith (Martinsried, Germany). Comparisons have been made
of the genome diversity within Haloquadratum populations in a
single saltern crystallizer pond as well as comparisons between
populations in similar environments at different geographic
locations. The pan-genome of Haloquadratum walsbyi is at
least 40 times the size of the genome of the type strain, and
genomic microdiversity within an extremely simple and rela-
tively constant environment is very high (17, 22, 40, 55). An
interesting study of experimental evolution was presented by
Jizhong Zhou (Norman, OK), using Desulfovibrio vulgaris as a
MEETING REVIEW 6973
model organism and monitoring genetic changes after expo-
sure of this nonhalophilic bacterium to 0.25 M NaCl for 1,000
generations. Salt-specific mutations and deletions were de-
tected in the salt-resistant phenotype, which used different
amino acids as osmoprotectants (35).
Genome sequencing of new isolates is getting simpler and
cheaper and will probably soon become routine. Undoubtedly,
this development will have profound implications on the tax-
onomy of the halophiles. Until taxonomy can be based on
comparison of complete genome sequences, multilocus se-
quence analysis (MLSA) is gaining popularity for the compar-
ison of strains for taxonomic and evolutionary studies. Thane
Papke (Storrs, CT) presented his extensive MLSA data on
Halorubrum isolates from Spain and Algeria. Analysis of the
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data indicates very frequent occurrence of homologous recom-
bination, to the extent that alleles were randomly associated, as
typical of sexually reproducing species. Natural competence
and conjugation (like the mating mechanism in Haloferax) (3)
may be the possible mechanisms for lateral gene transfer (61).
Emma White (Storrs, CT) and Hiroaki Minegishi (Saitama,
Japan) showed how analysis of the RNA polymerase subunit
B⬘(rpoB⬘) gene can help in reconstructing the phylogeny of the
Halobacteriaceae (51). Also for the Halomonadaceae, MLSA is
becoming a valuable tool for taxonomic studies, as shown by
Antonio Ventosa (Seville, Spain). For both groups, sets of
genes and primers have been defined that give good results
consistent with other genotypic and phenotypic traits.
The list of sequenced genomes of halophilic and halotoler-
ant Bacteria is as yet short. It does not yet even include
Halomonas elongata, the organism that, since it was described
30 years ago (89), has become one of the most popular model
organisms and has also found biotechnological applications
(30, 57). Its genome sequence will soon be published. Genome
sequence information is available for the anoxygenic halophilic
phototroph Halorhodospira halophila, for an extremely salt-
tolerant alkaliphilic sulfur-oxidizing bacterium of the genus
Thioalkalivibrio, for the thermophilic anaerobic halophile
Halothermothrix orenii, and for the aerobic heterotrophic Chro-
mohalobacter salexigens (58) and Salinibacter ruber.
Extensive environmental genomics data have been collected
for Salinibacter. Josefa Antón (Alicante, Spain) showed a high
degree of genomic variation within Salinibacter populations.
Comparative analyses indicate that Salinibacter ruber genomes
present a mosaic structure with conserved and hypervariable
regions. Overall, 10% of the genes encoded in the genome of
the Salinibacter M8 genome are absent from the type strain
Salinibacter M31. Metabolomic profiles also differed in these
two isolates (62).
HALOPHILIC VIRUSES
The Halophiles 2001 and 2004 symposia in Seville and
Ljubljana will be remembered as the events where the impor-
tance of fungi in hypersaline ecosystems became clear. Halo-
philes 2010 can then be described as the congress presenting
the importance of viruses. Phages attacking extremely halo-
philic Archaea were first described already in 1974 (83), but the
role of viruses in hypersaline ecosystems remained largely un-
explored.
Elina Roine (Helsinki, Finland) and her colleagues have
6974 MEETING REVIEW
discovered novel types of viruses attacking halophilic Archaea.
The isolation and characterization of pleomorphic viruses pos-
sessing a lipid envelope, containing either a single-stranded or
double-stranded DNA genome, show that viral diversity in
hypersaline environments (63, 64, 69) is much larger than pre-
viously assumed. Shaun Heaphy (Leicester, United Kingdom)
presented two novel lytic head/tailed viruses (virus BJ1 of the
Siphoviridae and virus BJ2 of the Myoviridae), infecting
Halorubrum kocurii, isolated from a salt lake in Inner Mongo-
lia (59). Few archaeal virus genomes have been sequenced, and
the complete sequence of virus BJ1 (EMBL accession number
AM419438) is therefore a welcome addition.
First results of a comprehensive study of viral distribution
and diversity in Great Salt Lake, UT, were presented by Bon-
nie Baxter (Salt Lake City, UT). Saltern crystallizer ponds are
also ideal environments to study virus diversity and dynamics,
as protozoa and other predators are absent, and numbers of
prokaryotes and virus-like particles are extremely high, typi-
cally in the order of ⬎107/ml and ⬎108 to 109/ml, respectively.
Forest Rohwer (San Diego, CA) showed his studies of virus
dynamics in such salt-saturated ponds. At first sight, the salt-
erns present predictable and stable communities of both Ar-
chaea and viruses, apparently different from the “kill-the-win-
ner” behavior, with rapid cycling of microbial taxa and their
viral predators that may be expected in such an environment
(67). Metagenomic analysis of the viruses in the salterns near
San Diego showed that the distribution of microbial taxa and
viral taxa remained stable over time but with strong dynamic
fluctuations of the prevalence of microbial strains and viral
genotypes. Thus, at the fine level, the populations of both
individual strains and viral genotypes fluctuate in a kill-the-
winner fashion (67).
Activity of viruses also may have profound implications on
the distribution of the extremely halophilic bacterium Salini-
bacter (Bacteroidetes). Josefa Antón (Alicante, Spain) studied
the metagenome of viral assemblages of saltern pond in which
Salinibacter accounts for around 15% of the prokaryotic com-
munity. Based on bioinformatic analysis (G⫹C content and
dinucleotide frequency analysis), about 24% of the retrieved
viral sequences could correspond to Salinibacter phages (70). It
seems that phages infecting Salinibacter are more active in the
environment than phages infecting Haloquadratum, and this
may possibly explain why Haloquadratum outnumbers Salini-
bacter in every environment that supports growth of these
organisms.
HALOPHILIC FUNGI
The importance of halophilic fungi, long neglected as mem-
bers of hypersaline ecosystems, became recognized only in the
past decade. Nina Gunde-Cimerman (Ljubljana, Slovenia)
gave an overview of the biology of the most widespread and
most halophilic or halotolerant fungi and yeasts. These include
the black yeasts Hortaea werneckii which grows up to 5 M NaCl,
the true halophile Wallemia ichthyophaga that requires at least
1.5 M NaCl and grows up to saturation, and Aureobasidium
pullulans that grows up to 3 M NaCl. All of these are com-
monly found in hypersaline lakes and in a great variety of
other, often unexpected, environments: domestic dishwashers,
polar ice, and possibly even on spider webs in desert caves (32).
APPL. ENVIRON. MICROBIOL.
The halophilic and halotolerant fungi use polyols such as
glycerol, erythritol, arabitol, and mannitol as osmotic solutes
and retain low salt concentrations in their cytoplasm. Molec-
ular studies on osmotic adaptation of Hortaea werneckii and
Wallemia ichthyophaga were presented by Ana Plemenitaš and
Janja Zajc (Ljubljana, Slovenia). Identification and structural
features of Na⫹-sensitive 3⬘-phosphoadenosine-5⬘-phos-
phatase HwHal2, one of the putative determinants of halotol-
erance in H. werneckii and a promising transgene to improve
halotolerance in crops, was presented (87). An in-depth un-
derstanding has been obtained of the HOG (high osmolarity
glycerol) pathway, and this understanding may be applied in
the future to the development of improved salt-resistant crops.
Glycerol-3-phosphate dehydrogenase is involved in glycerol
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synthesis by both Wallemia and Hortaea, and heterologous
expression of the gene encoding the enzyme can restore
halotolerance in Saccharomyces cerevisiae deficient in glycerol
production.
LONG-TERM SURVIVAL OF HALOPHILES
When brines dry out and halite crystals are formed, small
fluid inclusions remain entrapped within the crystals. Microor-
ganisms that inhabited the brine may get entrapped in these
inclusions (9). Since the first controlled studies showed that
such microorganisms may retain their viability for long periods
(54), the question of the longevity of different types of halo-
philes within salt crystals has become a popular topic, relevant
to disciplines including geology, biogeography, evolution, and
even space exploration (48).
Terry McGenity (Colchester, United Kingdom) presented
field studies and laboratory simulations of entombment of dif-
ferent types of microbes inside salt crystals. Salinibacter alone
survives poorly within halite crystals, but when it was trapped
inside a crystal together with Haloquadratum, longevity was
much enhanced. Thus, simple food chains and mutual interac-
tions occur between microorganisms in fluid inclusions in salt.
Examination of halite cores from Saline Valley, CA, repre-
senting salt deposited up to 150 thousand years ago, showed
remnants of algae within fluid inclusions entrapped in the salt
crystals. Morphological features as well as sequences of the
internal transcribed spacer between the 18S and 5.8S rRNA
genes led to the identification of Dunaliella, Ulothrix, and
Nephroselmis, as shown by Krithivasan Sankaranarayanan
(Binghamton, NY), who won first prize for his presentation by
a young scientist. Presence of entrapped algae, with their high
content of organic compatible solutes, may provide carbon and
energy sources enabling halophilic heterotrophic microorgan-
isms to survive for prolonged times (75).
OSMOTIC ADAPTATION, COMPATIBLE SOLUTES, AND
ADAPTATION OF INTRACELLULAR PROTEINS
TO SALT
There are basically two strategies that enable halophilic and
halotolerant microorganisms to live in high salt concentrations.
The “high-salt-in” strategy (used by the Halobacteriaceae,
Salinibacter, and the anaerobic Halanaerobiales) requires all
intracellular proteins to be stable and active in the presence of
molar concentrations of KCl and other salts. The “low-salt,
VOL. 76, 2010
organic-solutes-in” strategy is based on the biosynthesis and/or
accumulation of organic solutes that do not interfere greatly
with the activity of normal enzymes. But even such organisms
need to have salt-adapted proteins in the membrane exposed
to the saline medium. It is remarkable that already in the early
1930s Baas Becking concluded that Dunaliella must have a
highly acidic surface, based on the insensitivity of the alga to
certain otherwise toxic anions (8).
Over the years, Haloarcula marismortui has been the most
popular model organism for the study of the behavior of pro-
teins active in a high-salt environment. These include the Halo-
arcula ribosome, whose structure elucidation by Ada Yonath
was awarded the Nobel Prize for Chemistry in 2009. Christine
Ebel (Grenoble, France) presented an overview of molecular
adaptations of halophilic proteins, based on her studies of the
Haloarcula marismortui malate dehydrogenase and other en-
zymes. Particularly, the very acidic surface of the macromole-
cule allows protein-salt interactions that avoid water or salt
enrichment at the surface of the protein at high salt and pre-
serve its solubility (25, 44).
Volker Müller (Frankfurt, Germany) uses Halobacillus halo-
philus as a model to understand the mechanisms of osmotic
adaptation by a bacterium that accumulates organic-compati-
ble solutes. Using techniques of biochemistry, genomics, DNA
microarrays, etc., his group studies the way the organism senses
its environment. Halobacillus is the first chloride-dependent
bacterium reported, and several cellular functions depend on
Cl⫺ for maximal activities, the most important being the acti-
vation of solute accumulation. Halobacillus switches its os-
molyte strategy with the salinity in its environment by the
production of different compatible solutes. Glutamate and glu-
tamine dominate at intermediate salinities, and proline and
ectoine dominate at high salinities. Chloride stimulates expres-
sion of the glutamine synthetase and activates the enzyme. The
product glutamate then turns on the biosynthesis of proline by
inducing the expression of the proline biosynthetic genes (71,
72). Halobacillus dabanensis is used by Su-Sheng Yang and his
colleagues (Beijing, China) as a model organism to study the
genes involved in halotolerance, including genes encoding
Na⫹/H⫹ antiporters, enzymes involved in osmotic solute me-
tabolism, and stress proteins (27, 90). Studies of a mutant of
Halomonas elongata deficient in ectoine synthesis by Elisabeth
Witt (Bonn, Germany) showed the production of a new cyclic
compatible solute, 5-amino-3,4-dihydro-2H-pyrrole-2-carboxyl-
ate (ADPC). It is made by a side reaction of ectoine synthase
(EctC) that forms ADPC by cyclic condensation of glutamine.
She also demonstrated that ectoine synthase is a reversible
enzyme, which has its equilibrium (in case of ectoine synthesis)
completely on the side of the cyclic condensation product.
Ectoine and hydroxyectoine biosynthesis is widely found in
halophilic and halotolerant microorganisms, and the expres-
sion of the ect structural genes is induced by salt stress. But the
solutes provide protection not only against salt stress but also
against temperature stress in Bacillus subtilis and other salt-
tolerant bacilli, as shown by Erhard Bremer (Marburg, Ger-
many). Quantification of the intracellular ectoine concentra-
tion in Virgibacillus pantothenticus revealed that its production
is triggered either by an increase in external salinity or by a
reduction in growth temperature. Transcription of the ectoine
biosynthetic operon (ectABC) was enhanced under both envi-
MEETING REVIEW 6975
ronmental conditions (38). The crystal structure of Virgibacillus
salexigens EctD, the enzyme responsible for conversion of
ectoine to hydroxyectoine, is now known in detail (66).
LIPIDS, MEMBRANE-BOUND PIGMENTS, AND
MEMBRANE-LINKED PROCESSES
The cytoplasmic membranes of halophilic Archaea of the
family Halobacteriaceae contain interesting ether lipids and
often have retinal proteins (bacteriorhodopsin, halorhodopsin,
and sensory rhodopsins). Interesting lipids and retinal proteins
have also been found in Salinibacter.
Heiko Patzelt (Muscat, Oman) showed that unsaturated
ether lipids are far more common in the halophilic Archaea
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than generally assumed. Such unsaturated diether lipids were
earlier reported from the psychrotolerant haloarchaeon
Halorubrum lacusprofundi (29). Isolates of Haloarcula spp. and
Haloferax sp. obtained from a potash mine crystallization pond
in north Germany had unsaturated ether lipids up to 37% of
the total membrane lipid content. Only the phospholipids were
unsaturated, and these contained mostly four or six double
bonds in the archaeol chain.
Novel types of acylhalocapnines were described by Angela
Corcelli (Bari, Italy). Salisaeta longa, an organism that requires
lower salt concentrations than the related Salinibacter (Bacte-
roidetes), contains the hydroxyl fatty acid ester of 2-carboxy-2-
amino-3,4-hydroxy-17-methyloctadec-5-ene-1-sulfonic acid, a
sulfonate sphingoid base for which the common name of halo-
capnine is suggested (12). Salinibacter contains similar acylha-
locapnine lipids in its membrane, as well as a retinal protein
named xanthorhodopsin and an unusual ketocarotenoid
named salinixanthin, found in a 1:1 molar ratio with the retinal
pigment. Janos Lanyi (Irvine, CA) showed how the two chro-
mophores interact and how the carotenoid acts as an antenna,
transferring the absorbed light energy to the xanthorhodopsin
proton pump. Such an energy transfer phenomenon appears to
be unique for the clade that includes xanthorhodopsin as it is
not found between the carotenoid bacterioruberin and bacte-
riorhodopsin in Halobacterium and related genera. The effi-
ciency of the energy transfer is about 50%. The three-dimen-
sional structure of the xanthorhodopsin-salinixanthin system
has been determined from X-ray diffraction of xanthorhodop-
sin crystals, showing how the carotenoid interacts with the
retinal protein (42).
The Haloquadratum walsbyi genome encodes two different
bacteriorhodopsins. Both are expressed in the cells. Angela
Corcelli (Bari, Italy) reported the isolation of the two forms of
bacteriorhodopsin from Haloquadratum cultures using a bio-
chemical approach. Bacteriorhodopsin was also recovered
from biomass collected from the saltern crystallizer ponds of
the Margarita di Savoia saltern.
Mecky Pohlschröder (Philadelphia, PA) presented recent
results pertaining to mechanisms of protein transport across
haloarchaeal cytoplasmic membranes. In haloarchaea, al-
though the Sec pathway transports important substrates, in-
cluding subunits of type IV pilus-like structures, the Tat path-
way is used extensively and transports a wide range of secreted
proteins, the majority of which appear to be anchored to the
haloarchaeal membrane via a lipid anchor. In silico analyses
suggest that prominent use of the Tat pathway as well as
6976 MEETING REVIEW
extensive anchoring of Tat substrates via a lipid anchor is
unique to halophilic Archaea (the latest views on the mem-
branal mechanisms of protein secretion in Haloferax volcanii).
The Sec pathway remains an essential mode of protein trans-
port in halophilic Archaea (80, 84). Novel programs allowing
more accurate predictions of protein subcellular location (pub-
licly available at SignalFind.org) were also presented.
DNA REPLICATION, TRANSCRIPTION, TRANSLATION,
AND POSTTRANSLATIONAL MODIFICATION IN
HALOPHILIC ARCHAEA
Relatively few talks dealt with the molecular biology of halo-
philes and the basic properties of the DNA replication, tran-
scription, and translation machinery in different groups of
halophiles.
Stuart MacNeill (St. Andrews, United Kingdom) presented
novel information on the structure of the replication fork of
Haloferax. Haloferax volcanii encodes a single minichromo-
some maintenance protein. Its N-terminal domain has a puta-
tive DNA-binding ␤-hairpin, a Cys4 zinc ribbon, and a ␤-hair-
pin with a role in interdomain communication. Genetic
analysis of different mutants enabled the elucidation of the
roles of the different proteins associated with the replication
fork (43).
The biosynthesis and assembly of gas vesicles in halophilic
Archaea have been used as a model for the study of transcrip-
tion and other molecular processes in the Halobacteriaceae for
nearly 3 decades now. Felicitas Pfeifer (Darmstadt, Germany)
presented the latest information how the Halobacterium sali-
narum gas vesicle, when expressed in Haloferax volcanii, can be
used as a convenient model system for the study of gene ex-
pression, transcription, and translation. Gas vesicles are com-
posed of two structural proteins: the hydrophobic GvpA that
forms the core of the cylinders and the hydrophilic GvpC that
cross-links the GvpA subunits at the outside and provides
strength to the vesicles. GvpC is now also known to be involved
in the determination of the shape of the vesicles. Anaerobiosis
inhibits gas vesicle formation. Fourteen gvp genes are required
for gas vesicle formation, and these are arranged in two oppo-
sitely organized clusters. The function of the different promot-
ers and transcriptional activators is becoming increasingly clear
(13, 36, 81).
Updates about the molecular mechanisms of translational
control in Halobacterium salinarum and Haloferax volcanii were
given by Jörg Soppa (Frankfurt, Germany). Different mecha-
nisms for translation initiation are known: (i) interaction be-
tween 16S rRNA and a Shine-Dalgarno sequence, (ii) the
eukaryotic mechanism of linear scanning of the small ribo-
somal subunit from the 5⬘-cap to the start codon, (iii) an
alternative eukaryotic mechanism using internal ribosomal en-
try sites, and (iv) leaderless transcripts that require an undis-
sociated ribosome and the initiator tRNA (a mechanism en-
countered in all three domains of life). Characterization of the
5⬘ and 3⬘ ends of haloarchaeal transcripts showed that the
majority of the transcripts are leaderless, that Shine-Dalgarno
sequences are very rare, and that about a third do not fall in
any of these four classes and must use a novel, yet uncharac-
terized method of translation initiation (19).
Posttranslational modification is studied in the laboratory of
APPL. ENVIRON. MICROBIOL.
Jerry Eichler (Beer-Sheva, Israel), centering on the biosynthe-
sis of the glycoproteins so abundantly found in the cell enve-
lope of the Halobacteriaceae. Asn-modified glycoproteins are
common in Archaea, and their production was studied using
Haloferax volcanii as a model. A series of agl (archaeal glyco-
sylation) genes was defined, encoding proteins involved in the
assembly and attachment of a novel pentasaccharide to Asn
residues of the S-layer glycoprotein. The functions of several
Agl proteins are now known (1, 2, 45, 91).
GENETIC SYSTEMS FOR HALOPHILIC PROKARYOTES
Two interesting systems for genetic manipulation of halo-
philes were highlighted at the meeting. Already in the original
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species description of Haloferax volcanii the formation of in-
tercellular bridges was noted (52). Moshe Mevarech (Tel Aviv,
Israel) presented a survey of the genetic manipulation of
Haloferax volcanii, developed since genetic transfer based on
cell mating was first described 25 years ago (50). The mating
system of Haloferax volcanii resembles eukaryotic sexual mat-
ing rather than bacterial lateral gene transfer. Large amounts
of genetic material can be transferred this way (3). The suc-
cessful mating of Haloferax volcanii and Haloferax mediterranei,
yielding hybrid progeny, was announced.
Saskia Köcher (Frankfurt, Germany) presented a (prize-
winning) poster describing the establishment of a genetic sys-
tem for the manipulation of Halobacillus halophilus, based on
protoplast fusion and markerless gene disruption. Cells can be
transformed by protoplast transformation, resulting in integra-
tion of a nonreplicating plasmid via single homologous recom-
bination. The method was used to generate proline biosynthe-
sis mutants. This genetic manipulation strategy will now open
the way to study many more properties of Halobacillus at the
genetic level.
BIOTECHNOLOGICAL APPLICATIONS
OF HALOPHILES
In comparison to other groups of extremophilic microorgan-
isms such as the thermophiles and the alkaliphiles, the halo-
philes of all three domains have been relatively little exploited
in biotechnological processes, with notable exceptions of ␤-car-
otene from Dunaliella, bacteriorhodopsin from Halobacterium,
and ectoine from Halomonas (57). The biotechnology section
of the meeting focused on production/modification techniques
of compatible solutes, bioplastics, and halophilic enzymes. In
addition, attention was drawn toward secondary metabolites
from halophiles as well as bioremediation and biofuel produc-
tion.
One success story of halophile biotechnology is the produc-
tion and application of the compatible solute ectoine, currently
produced at large scale by bitop AG in Germany using “bac-
terial milking” of Halomonas elongata. Ectoine is the active
ingredient of many cosmetics and skin care products and in-
creasingly becomes important in medicinal preparations (30).
In addition, ectoine (and/or suitable derivatives) is used as a
protectant for biomolecules and enhancer in molecular biology
applications such as PCR and DNA microarray techniques (47,
74). Erwin Galinski (Bonn, Germany) presented a survey of
the industrial production processes of ectoine and, in particu-
VOL. 76, 2010
lar, a critical analysis of the maximal specific production rates
obtainable with H. elongata as the production strain (50 mg g⫺1
of dry weight h⫺1 at 5 to 7.5% NaCl). Different strategies
have been applied in attempts to increase production, in-
cluding heterologous expression of the ectoine gene cluster
in Escherichia coli and concomitant overexpression of genes
that increase the supply of limiting precursors for ectoine
biosynthesis, thus bypassing “metabolic bottlenecks“ (15,
76). Heterologous expression of the ectoine gene cluster in
E. coli is at present not a suitable alternative to ectoine
production in H. elongata. With respect to the hydroxylated
derivative (S,S-␤-hydroxyectoine) the situation is, however,
different. As this compound is always produced in a mixture
with ectoine in H. elongata, a costly chromatographic sepa-
ration is required. By overexpressing the ectD gene (encod-
ing ectoine hydroxylase) in E. coli, an efficient whole-cell
biotransformation system for ectoine has been established
in which the product (hydroxyectoine) leaked out of the
cells and accumulated in the medium (E. A. Galinski, M.
Stein, A. Ures, and T. Schwarz, World patent application
WO 2009/059783 A1). Novel developments concern use of
genetically engineered H. elongata for production of rare
and thus far inaccessible compatible solutes. The potential
of this approach for the development of new production
processes was demonstrated using the compatible solutes
mannosylglycerate (gene cluster from the thermophilic
Rhodothermus marinus) and N-acetyl-glutaminyl glutamine-
1-amide (gene cluster from Pseudomonas putida) as exam-
ples.
Whereas in past meetings the production of extracellular
halophilic polymers with interesting rheological properties had
claimed attention, the emphasis of this year’s meeting (as re-
gards polymers) has clearly been on intracellular polyesters.
Production of poly-␤-hydroxyalkanoates—biodegradable poly-
mers with plastic-like properties—although not restricted to
halophilic prokaryotes, was the topic of no less than four talks
and a number of posters. Some halophilic or halotolerant Bac-
teria were shown to be excellent producers of such bioplastics.
One of these is Halomonas boliviensis, as argued by Jorge
Quillaguamán (Cochabamba, Bolivia), who presented strate-
gies to optimize the biosynthesis of such bioplastics coupled
with production of the high-value products ectoine and hy-
droxyectoine (65, 86). Archaea of the genus Haloferax are also
known as poly-␤-hydroxyalkanoate producers and the biosyn-
thetic pathway leading to their production were elucidated by
Hua Xiang and colleagues (Beijing, China) (33, 41). Unfortu-
nately none of the presenters compared the potential of halo-
philic producers with the current productivity of industrial
strains as used, for example, by Metabolix/ADM (Cambridge,
MA) for their bioplastic product Tirel.
Many alkaliphiles are halophilic as well, and many useful
enzymes applied in the detergent industry (washing powders),
the textile industry, and other processes were derived from
bacteria growing in saline alkaline lakes. Brian Jones (Leiden,
Netherlands) explained how the saline alkaline lakes in Kenya
and Inner Mongolia have been a rich source of organisms
and/or genes from metagenomic libraries, and some of these
are already explored as starting material for the production of
commercially valuable enzymes, in particular, proteases and
amylases.
MEETING REVIEW 6977
Halophilic enzymes (typical for Archaea and Salinibacter but
also for exoenzymes of any halophile) are characterized by an
excess of acidic amino acids and subsequent negative surface
charge. This peculiarity allows effective competition for hydra-
tion water and enables function in solutions of low water ac-
tivity, including organic solvent/water mixtures. The immediate
advantages for enzyme technology are as follows: increased
salt and heat tolerance, a catalytic environment which enables
use of less polar educts, and potential reversal of hydrolytic
reactions, all of which make them strong candidates for indus-
trial biocatalysts.
An increasingly important industrial application of enzymes
is the environmentally friendly production of stereo-specific
building blocks for pharmaceuticals in “white biotechnology.”
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One such example, the stereo-specific production of alcohols
from ketones was presented by Leanne Timpson and her col-
leagues Ann-Kathrin Liliensiek and Francesca Paradisi (Dub-
lin, Ireland). Halobacterial alcohol dehydrogenases were over-
expressed in Haloferax volcanii, using novel expression systems
(4, 39). A number of poster presentations outlined the search
for useful enzymes such as proteases, cellulases, lipases, amy-
lases, and mannanases from halophiles, including isolates from
Chinese and Iranian lakes, and a prize-winning presentation by
Yasuhiro Shimane and colleagues (Saitama, Japan) on en-
zymes derived from haloarchaea isolated from domestic and
commercial salt samples.
Nayla Munawar and Paul Engel (Dublin, Ireland) ap-
proached protein engineering of substrate specificity in a halo-
philic enzyme by site directed mutagenesis in the absence of a
crystal structure of the enzyme. Using the crystal structure and
previous mutagenesis of a mesophilic counterpart (Clostridium
symbiosum glutamate dehydrogenase) as a guide, they selected
corresponding residues in Halobacterium salinarum glutamate
dehydrogenase (GDH) for site-directed mutagenesis and cre-
ated a novel halophilic dehydrogenase which accepts L-methi-
onine, L-norleucine, and L-norvaline as substrates instead of
glutamate.
Secondary metabolites and, in particular, the untapped po-
tential of halophilic actinomycetes as a source for novel anti-
biotics are increasingly becoming important, as explained by
Wen-Jun Li (Kunmin, China). The abundance of culturable yet
unknown types was beyond expectation, with predominance of
Nocardiopsis, Saccharomonospora, and Streptomonospora. In
the context of new drug discoveries, Xiukun Lin (Qingdao,
China) reported on novel compounds from actinomycetes iso-
lated from salterns and their cytotoxic effect against a range of
cancer cell lines.
The worldwide problem of petroleum contamination and
potential application of halophiles for bioremediation were
addressed by Mohammad Amoozegar (Tehran, Iran), who de-
scribed a novel isolate, similar to Alcanivorax dieselolei, able to
grow on crude oil, diesel fuel, and pure aliphatic hydrocarbons
but unable to degrade aromatic compounds. Its use in saline
soils was investigated. A consortium of at least six culturable
strains (including Marinobacter and Halomonas sp.) was able to
degrade various polyaromatic hydrocarbons over a salinity
range from 1 to 17% NaCl. Thus, the degrading potential of
halophiles has just started to come to light and will become
increasingly important in the future.
Another process in which halophiles may contribute in the
6978 MEETING REVIEW
future is the production of biofuel. Melanie Mormile (Rolla,
MO) explained how halophilic/haloalkaliphilic and halotoler-
ant bacteria could be used to break down biomass material and
form biofuel products. Lignocellulosic biomass as a source for
fermentative production of biofuel products, such as ethanol
and hydrogen, may become a commercially interesting option,
provided lignin components can be removed. The required
alkaline pretreatment (to remove lignin) and subsequent par-
tial neutralization will create an environment for halophilic or
haloalkaliphilic fermentative bacteria in cellulose-converting
processes. The general trend toward use of algae for biofuel
(biodiesel) production is problematic because of the high con-
sumption of fresh water. The use of halophilic algae may over-
come such hurdles by means of efficient nonpotable water
recycling and open up a bright future for halophile technology.
It is thus possible that in the future the biotechnological
application of halophiles, or of genes derived from them, will
extend to many more members of this extremely diverse group
of microbes. Possible areas of exploitation may stretch from
production of valuable compounds and remediation of con-
taminated waters and soils to future solutions of the world’s
liquid fuel crisis.
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Yanhe Ma is a Professor of Microbiology
and the Vice-Director of State Key Labora-
tory of Microbial Resources in the Institute
of Microbiology, Chinese Academy of Sci-
ences (CAS). He is also the Vice-Director
of the newly founded Tianjin Industrial Bio-
technology R&D Center, CAS. He is the
Deputy Secretary-General of the Council of
Chinese Society of Biotechnology and the
Vice-President of the Beijing Society for
Microbiology. He is also a member of the
International Committee on Systematics of Prokaryotes (ICSP) Sub-
committee on Taxonomy of Halobacteriaceae. In addition, he is Asso-
ciate Editor of Saline Systems and of the Chinese Journal of Bioprocess
Engineering. He won the Invention Award of the Chinese Academy of
Sciences in 1999 and the National Award of Advanced Science and
Technology in 2000. His research interests are mainly in the biodiver-
sity, physiology, and application of extremophiles.
Erwin A. Galinski studied biology, chemis-
try, and biochemistry at Bonn University
and at the University of St. Andrews (Scot-
land) as a scholar of the German National
Merit Foundation. He received his Dr. rer.
nat. degree in microbiology (1986) and his
university lecturer qualification in microbi-
ology and biotechnology (1993) from Bonn
University. After a period as tenured Pro-
fessor of Biochemistry/Biotechnology at
Münster University (1997 to 2001), he re-
turned to the Rheinische Friedrich-Wilhelms University in Bonn as
full Professor of Microbiology. He has held the positions of Head of
the Examination Committee, Member of the Faculty Council of Nat-
ural Sciences, and Chairman of the Biology Section and the Student
Fees Financial Board. He is currently Managing Director of the De-
partment of Microbiology and Biotechnology. His main interests are in
osmoprotective mechanisms of halophilic bacteria, in particular, pro-
duction and application of compatible solutes such as ectoines (ingre-
dient of skin care products), genetic engineering of salt tolerance, and
principles of anhydrobiosis.
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fed-batch culture and milking process. J. Biotechnol. 147:46–51.
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nas elongata, a new genus and species of extremely salt-tolerant bacteria. Int.
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philic bacterium Halobacillus dabanensis D-8T: cloning and molecular char-
acterization. FEMS Microbiol. Lett. 255:89–95.
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coprotein. Mol. Microbiol. 69:1234–1245.
William D. Grant was born in Scotland in
1942. He received his B.Sc. (1964) and
Ph.D. (1968) from the University of Edin-
burgh. After postdoctoral studies at the
University of Wisconsin, Madison, WI, he
returned to the United Kingdom as a re-
search fellow at the University of Leicester,
subsequently becoming Professor of Envi-
ronmental Microbiology, latterly Emeritus
Professor of Environmental Microbiology.
Since the late 1970s Dr. Grant has been
interested in microbial biodiversity in extreme environments, particu-
larly in East African saline and soda lakes. He has also worked on the
diversity of microbes in salt mines, ancient salt deposits, and low-level
nuclear waste. His current interests are mainly in the molecular ana-
lyses of microbes and microbial signatures in hypersaline environments
and accessing microbial genetic resources without the need for culture.
Aharon Oren (born 1952 in Zwolle, Neth-
erlands) received his M.Sc. (1974) from the
University of Groningen and his Ph.D.
(1978) from the Hebrew University of Jeru-
salem, Israel, where he has been a full pro-
fessor since 1996. He serves as editor of
International Journal of Systematic and En-
vironmental Microbiology, Extremophiles,
FEMS Microbiology Letters, and Saline Sys-
tems. He is Executive Secretary/Treasurer of
the International Committee on Systematics
of Prokaryotes and member of the ICSP Subcommittees on the
Taxonomy of Halobacteriaceae, Photosynthetic Prokaryotes and
Halomonadaceae, President of the International Society for Salt Lake
Research, and board member of the Israel Society for Microbiology.
He received the Moshe Shilo Prize (1993) and the Ulitzki Prize (2004)
of the Israel Society for Microbiology and is a Fellow of the American
Academy of Microbiology (2000). In 2010 he was awarded an honorary
doctorate from the University of Osnabrück. His research focuses on
the ecology, physiology, and taxonomy of halophilic microorganisms.
VOL. 76, 2010 MEETING REVIEW 6981

Antonio Ventosa is Professor and Head of

the Department of Microbiology and Parasi-
tology of the University of Seville, Spain. He
has been Vice-Dean (1993 to 1997) and Dean
(1997 to 2001) of the Faculty of Pharmacy
and Vice-Rector of Postgraduate Studies
(2003 to 2006) of his university. He is asso-
ciate editor of the International Journal of
Systematic and Evolutionary Microbiology
and editorial board member of Systematic
and Applied Microbiology, Extremophiles, In-
ternational Microbiology, and Archaea. He is a member of the Interna-
tional Committee on Systematics of Prokaryotes (ICSP) and Chairman
of the ICSP Subcommittees on the Taxonomy of Halobacteriaceae and
Halomonadaceae. He won the Jaime Ferran Award (the Spanish So-
ciety of Microbiology, 1991) and the FAMA Research Prize (Univer-

Downloaded from http://aem.asm.org/ on April 30, 2021 by guest

sity of Seville, 2008). He is a Fellow of the American Academy of
Microbiology (2004) and the European Academy of Microbiology
(2009). His research focuses on extremophilic microorganisms, micro-
bial diversity of hypersaline environments, taxonomy and phylogeny,
and biotechnological applications of halophiles.