Pereira2017 Diversidade Amazonia

Chapter 5
Overview on Biodiversity, Chemistry,

and Biotechnological Potential
of Microorganisms from the Brazilian Amazon
Jose Odair Pereira, Antonia Queiroz Lima de Souza, Afonso Duarte Leão de

Souza, Suzelei de Castro França, and Luiz Antonio de Oliveira
Abstract Brazil is one of the most biodiverse countries on the planet and a part
expressive of that biodiversity are situated in the vast Amazon region. The biodiver-
sity of the Amazon is distributed in different environments represented by upland
forest, savanna, igapó forest, and floodplains. Microorganisms occur abundantly,
considering that all the natural vegetal coverage of soil is full of microorganisms
colonizing hosts and other microhabitats as water and animals. Owing to the fact
that microorganisms from the Amazon are little known, in this chapter, we intend to
present the current status of research on microorganisms in the Amazon, mainly
reviewing results of researches that have been carried out in the state of Amazon
J.O. Pereira (*)

Laboratory of Microbial Bioactives, Federal University of Amazonas –UFAM,
Av. Rodrigo Otávio, 6200, Manaus, AM 69077-000, Brazil
e-mail: jodair@ufam.edu.br
A.Q.L. de Souza
Laboratory of Food Microbiology, Federal University of Amazonas – UFAM,
A.D.L. de Souza
Department of Chemistry, Federal University of Amazonas – UFAM,
S. de Castro França
Biotechnology Division, University of Ribeirão Preto-UNAERP,
Av. Costábile Romano, 2201, Ribeirão Preto, SP 14096-900, Brazil
L.A. de Oliveira
Laboratory of Ecology and Biotechnology of Microorganisms, National Institute for
Researche in the Amazon –INPA, Av. André Araújo, 2936, Manaus, AM 69077-000, Brazil
© Springer International Publishing AG 2017 71

J.L. de Azevedo, M.C. Quecine (eds.), Diversity and Benefits of Microorganisms
from the Tropics, DOI 10.1007/978-3-319-55804-2_5
72 J.O. Pereira et al.
within the principal institutions. The microbiota associated with plants from
Amazon is an economically promising source of bioactives. In the state of Amazon,
there is an important microorganism culture collection, which is preserved in edu-
cation and research institutes. The biodiversity of microorganisms living in water
habitats of Amazonian rivers has been assessed via independent culturable methods
and with the help of molecular tools as well as the microbiota from rhizosphere.
Data from previously reported studies related to biological control assays conducted
with natural products from endophytic fungi, as well as results of research processes
addressing water and soil bioremediation, are discussed. Finally, a variety of micro-
bial metabolites uncovered by studies carried out by few regional groups, exploring
metabolites produced by bacteria and fungi from plants and other Amazonian
sources, are presented. Considering that the vast diversity of a few species of fungi
already described were from tropical countries, the exploration of the Amazon
microbiological diversity is of prime importance.
Keywords Amazonian rainforest • Endophytic microorganisms • Biorremediation •

Microbial culture collection • Guarana • Natural products • Rhizospheric microbiota
• Biodiversity
5.1 Introduction
The largest rainforest and the largest river basin in the world with 6.7 million and
6.9 million square kilometers, respectively, are situated in the vast Amazon region.
Over half of the forest area (4.1 million km2) is situated in Brazil. The biodiversity
of the Amazon is distributed in different environments represented by upland forest,
savanna, igapó forest, and floodplains, making Brazil one of the most biodiverse
countries on the planet. In those ecosystems, the richness of biodiversity is reflected
in its lush flora and fauna, encompassing 21,000 phanerogam species (ARPA 2004),
approximately 16,000 tree species (Steegeter et al. 2013). The animal biomass is
mainly formed by ants, over 3000 species found on trees; 3000 species of freshwa-
ter fish (Série Biodiversidade 31 2007); 1000 bird species of which 283 are consid-
ered rare (Série Biodiversidade 31 2007; ARPA 2004). It is predictable that
microorganism also occurs abundantly, considering that all the natural vegetal cov-
erage of the soil is full of microorganisms colonizing these hosts and other micro-
habitats as water and animals. Despite the huge genetic heritage very little is known
about the microbial diversity of the Amazon and its ecological relationships. This
rich microbiota demands academic investigations, focusing on the isolation and
identification of new species for scientific purposes and application in the develop-
ment of biotechnological processes for the production of bioactives of interest of the
health care and food industry and also for the development of bioproducts produced
by the agroindustry.
5 Overview on Biodiversity, Chemistry, and Biotechnological Potential… 73
Data on biodiversity, reported by The Brazilian Ministry of the Environment—

MMA in 2002, when Brazilian biomes were evaluated as well as data from the
ARPA project (Amazon Protected Areas) covering the period 2002–2010 do not
address the microbial diversity or the chemical studies on metabolites produced by
these organisms. The analysis of data on the Brazilian biodiversity within the period
1995–2005 (Manfio and Canhos 2004; Manfio 2005) revealed that only a small
group of researchers contributed for the knowledge of a few microbial genera. Most
of the research done was focused on taxonomic characterization of specific groups
of microorganisms and mostly using classical identification techniques based on
cultivation and morphological description data and sometimes metabolism and
physiology. Studies on environmental microbiology using independent methods of
cultivation with support of molecular tools were performed by restricted groups of
researchers in the country. During the period of completion of the survey, the best
record of taxonomic diversity was limited to filamentous fungi and encompassed a
small number of taxa.
Despite the fact that microorganisms, together with invertebrates, constitute
most of the biosphere species and play an important role in the maintenance of eco-
systems, they are still little known in Brazil (Maia et al. 2015) and abroad (Hamond
1995). Groups of microbial species recorded by Manfio (2005) in culture collec-
tions are shown in Table 5.1.
CNPq (Brazilian National Council for Technological and Scientific Development)
census 2010 recorded 265 research groups investigating microorganisms in Brazil
of which 16 in the Amazon. From these, only two groups investigate the chemical
composition of the microbiota and other four develop biotechnological processes.
All of the other groups’ research studies are focused on biodiversity features or on
agronomical and therapeutic uses of microbial products. The census of 2015 showed
an expansion of more than 100 groups working with microorganisms in Brazil,
though the location of those groups is not yet disclosed.
In this chapter, we intend to present the current status of research on microorgan-
isms in the Amazon, mainly reviewing results of researches that have been carried
out in the state of Amazonas within the principal research institutions, represented
Table 5.1 Known and estimated number of microbial species in relation to material deposited in
collections of culture
Approximate number of
species Available material in collection of cultures
Total per % of number of
Group Known Estimated group known species Estimated species
Algae 37,700–42,900 400,000 1.600 3.7–4.2 0.4
Bacteria 4300 1,000,000 2.300 53.5 0.2
Fungi 70,600–72,000 1,500,000 11.500 16.0–16.3 0.8
Virus 3600 400,000 2.200 61.1 5.5
Adapted from Manfio (2005)
by the Universidade Federal do Amazonas (UFAM), Universidade do Estado do

Amazonas (UEA), Instituto Nacional de Pesquisa da Amazonia (INPA), Instituto
Leonidas e Maria Deane (ILMD)-FIOCRUZ, and Embrapa Amazônia Ocidental-
(EMBRAPA). The researches comprising studies on the Amazon microbiota diver-
sity are not restricted to the work of researchers based in that region, since important
contributions by researchers from other Brazilian and foreign universities were
included. One example is the study “Conversion of the Amazon rainforest to
agriculture results in biotic homogenization of soil bacterial communities”
(Rodrigues et al. 2013), in cooperation with researchers from University of Texas,
University of São Paulo, University of Oregon, University of Massachusetts,
Embrapa Agrobiologia-Brazil, Centro de Energia Nuclear na Agricultura-
Piracicaba-Brazil, and Michigan State University.
5.2 Amazon Biodiversity
In the state of Amazonas, there are important collections of cultures of microorgan-

isms preserved in Education and Research Institutions. However, many of these
collections are not registered in international organizations and are maintained only
due to the interest of researchers. The contributions to such collections come from
research projects carried out by undergraduate and graduate students who share the
purpose of preserving microorganisms from the Amazonian biodiversity, which
produce substances with application in the food and pharmaceutical industry, and
that are useful for biodegradation of xenobiotic contaminants from the environment.
These collections also contain microorganisms of medicinal and agroforestry inter-
est. Since 1992, UFAM maintains a collection of endophytic microorganisms that
contains more than 3500 isolates obtained from various tropical hosts including
fruit trees as Theobroma grandiflorum (Willd. Ex Spreng) K. Schum (cupuaçu),
Theobroma cacao L. (cacao), Bactris gasipaes Kunth (pupunha), Mauritia flexuosa.
Mart (buriti), Paullinia cupana H.B.K. var. sorbilis (Mart.) Ducke (guaraná),
Euterpe oleracea. Mart. (açaí), Solanum sessiliflorum Dunal (cubiu), Passiflora cin-
cinnata Mast (maracujá do mato), Eugenia stipitata (Mark) Vaughn (araçá boi),
Annona muricata L. (graviola), Manihot esculenta Crantz (macaxeira); medicinal
plants as Aniba rosaeodora Ducke (pau rosa), Himatanthus sucuuba (Spruce) Wood
(sucuuba), Copaifera multijuga Hayne (copaíba), Dipteryx odorata (Aubl.) Willd.
(cumarú), Phyllanthus niruri L. (quebra-pedra), Bryophyllum pinnatum (Lam.)
Oken (corama), Arrabidaea chica Verlot (crajirú), Gustavia augusta L. (mucurão),
Peperomia pellucida (L.) Kunth (erva de jabuti), Piper peltata (L.) Miq. (capeba);
toxic plants such as Palicourea longiflora (Aubl.) Rich (erva de rato), Strychnos
cogens Benth, and S. toxifera R.H. Schomb. ex Lindl. (curari) and aquatic plants
such as Eichornnia crassipes (aguapé), Victoria amazonica (Poepp) Sowerby
(vitória régia), and Pistia stratiotes L. (alface de água doce). A large number of
Deuteromycetes and bacteria associated with basidiomycetos besides basidiomyce-
tos isolated from decaying wood of different forest environments are also
maintained in that collection. The endophytic microorganisms deposited in this col-

lection are mainly bacteria and fungi found inside plant tissues or organs of healthy
hosts. These microorganisms can colonize the inside of cells, the intercellular
spaces, xylem and phloem without causing damage or apparent symptoms in the
host (Azevedo et al. 2000, 2002; Stone et al. 2000; Souza et al. 2004; Borges et al.
2009; Lacava and Azevedo 2013, 2014; Sebastianes et al. 2013).
The interaction of endophytes especially with medicinal plants presents interest-
ing aspects mainly because when interacting microorganisms and their host plants
can undergo metabolic modifications giving rise to a number of bioactive molecules
with numerous biotechnological applications (Azevedo et al. 2002; Yu et al. 2010;
Rhoden et al. 2012; Nisa et al. 2015; Polli 2016).
The microbiota associated with plants from Amazon is an economically promis-
ing source of bioactives (Azevedo et al. 2000, 2002; Banhos 2016). Healthy native
plants from several regions of the state of Amazonas were selected for the isolation
of endophytic microorganisms, which have often been investigated for their bio-
technological potential (Souza et al. 2004). Studies with endophytes from plants
native to Amazon have been reported with several hosts like P. cupana (Guimarães
1998; Costa Neto 2009; Bentes and Costa Neto 2011), B. gasipaes (Costa Neto
2002; Rondon 2010), T. grandiflorum (Medeiros-Galvão 1998), T. cacao (Hanada
et al. 2008, 2009, 2010), M. esculenta (Rondon 2003), M. flexuosa (Koolen et al.
2012a); C. multijuga (Cassa-Barbosa 2001), H. sucuuba (Magalhães 2000),
Cecropia sp. (Cruz 2005), G. elliptica (Almeida 2014), Myrcia guianensis (Banhos
2011; Banhos et al. 2014), Duguetia stelechantha (Koolen et al. 2013), Rollinia sp.
(Souza 2012a), D. flagellaris Huber (Souza 2013), P. peltata and P. pellucida
(Marcon 2013), A. rosaeodora (Silva 2010); E. crassipes (Batista 2009; Araujo
2014), Victoria amazônica, P. stratiotes, P. longiflora, S. cogens (Souza 2001; Souza
et al. 2004; Souza et al. 2008), S. toxifera (Koolen 2011; Koolen et al. 2012b, 2014),
and Cladocolea micrantha (Guimarães et al. 2013). In general, it has been found
that the most common endophytes belong to genera Colletotrichum, Glomerella,
Fusarium, Guignardia, Phomopsis, Trichoderma, Penicillium, Aspergillus, and
Xylaria. Screening of T. grandiflorum fruits allowed the isolation of the endophyte
P. purpurogenum capable of producing red pigment, thermostable, photostable, not
susceptible to variations of pH and with high antioxidant potential. Also, endo-
phytic isolates from C. multijuga were able to produce two or more hydrolytic
enzymes. Moreover, microorganisms from P. longiflora, M. flexuosa, S. toxifera,
and from basidiomycetes, source of lignocellulolytic enzymes, were competent to
decompose regional agricultural waste (Silva 2013, 2015; Fernandes 2013).
On the other hand, many isolated microbial strains of various natural environ-
ments of the Amazon are deposited in well-established Culture Collections and
recorded in international bodies of reference. The Culture Collection DPUA was
established in 1974 at the Federal University of Amazonas (UFAM), in the city of
Manaus, Amazonas, Brazil. Currently, the collection is registered in the World Data
Center for Microorganism (WDCM) and in the World Federations of Culture
Collections (WFCC) under the number 715. This collection comprises 1566 cul-
tures preserved in mineral oil, Castellani method, and silica gel (Teixeira et al. 2011,
2015; Zanotto et al. 2012; Alecrim et al. 2015). Several studies account for the
biotechnological value of the DPUA culture collection (Silva et al. 2010a, b; Macedo
et al. 2011; Teixeira et al. 2012a, b; Duran et al. 2012; Barroncas et al. 2012; Fonseca
et al. 2014; Nascimento et al. 2014; Paiva et al. 2015).
The Laboratory of Amazon Microbial Diversity at the Leonidas and Maria Deane
Institute (ILMD)-FIOCRUZ AMAZON is responsible for important health
researches. The biological collection of this laboratory encompass bacteria and
fungi isolated from various Amazonian substrates such as soil, water, air, regional
fruit, and clinical field samples and according to its curator the collection contains
1455 microorganisms. Since 2003, this collection has been integrated to the
Information System of Collections of Biotechnological Interest (SICol) of the
Brazilian Ministry of Science and Technology and was also affiliated to the WFCC.
Another important collection is settled at the National Institute of Amazonian
Research (INPA), separated into two areas: microorganisms of medical interest
(since 1970) and microorganisms of silvicultural interest (since 1977), comprising
Rhizobia samples and lignocellulolytic fungi including edible species of fungi.
Currently, this collection incorporates 1830 fungal cultures (from wood decay and
plant pathogens) and 1680 cultures of bacteria obtained from Amazonian soil sam-
ples (pathogenic strains or those beneficial for agriculture). The collection of
microorganisms of medical interest consists of fungi, viruses, mycobacteria, and
Leishmania field strains and holds more than 6000 microbial isolates mostly of
them obtained from the Amazonian individuals. INPA researchers developed an
interesting approach for cultivation of edible mushrooms. These fungi are food-
stuffs rich in protein, vitamins, fiber, and present low levels of lipids. Nutritional
and therapeutic properties have been attributed to them due to their composition
(Furlani 2004; Furlani and Godoy 2005; Sales-Campos 2008). Several studies
have been conducted to assess the chemical composition and physicochemical
properties of fungal species cultivated on various wood substrates derived from
industrial activity and agro-industrial waste in the Amazon region (Sales-Campos
2008). In addition to the well-known species belonging to the genera Agaricus,
Pleurotus, and Lentinus widely commercialized (Eira 2004), many wild mush-
rooms, not yet commercially grown, can be explored. An example is the fungus
Lentinus strigosus known and consumed by Amazon population (Sales-Campos
and Andrade 2011; Andrade et al. 2013). Researchers at INPA work on the devel-
opment of techniques for preservation of fungal isolates (Sales-Campos et al.
2015); on the use of different regional substrates for the cultivation of fungi (Sales-
Campos et al. 2011a, b) and on the chemical profile of fungi (Sales-Campos et al.
2011a, b, 2013).
DNA markers have been considered a valuable tool on the identification of
microorganisms and to precisely estimate their genetic variability without influence
of the environment. Online databases of nucleotide sequences with available ITS
sequences and rDNA genes (18S, 5.8S, and 28s) of fungi are useful to perform mul-
tiple comparisons to identify genetic material from environmental isolates (Bernard-
Wenzel et al. 2010; Rhoden et al. 2012). Independent cultivation techniques
combined with analysis of RNA 16S gene, amplification of 16S rDNA, amplified
rDNA restriction analysis (ARDRA), denaturing gradient gel eletrophoresis
(DGGE), and terminal restriction fragment length polymorphism (T-RFLP) have
been useful to study bacterial communities from different environments (Dunbar
et al. 1999; Cottrel and Kirchman 2000; Smalla et al. 2001). Some authors state that
independent cultivation methods tend to substitute conventional methods for the
isolation, cultivation, screening, and comparison among microbial communities
(Hugenholtz and Pace 1996; Hugenholtz et al. 1998).
A collaborative project between the College of Agriculture “Luiz de Queiroz”—
ESALQ and UFAM, with financial support from both the State of São Paulo
Research Foundation (FAPESP) and the State of Amazonas Research Foundation
(FAPEAM) resulted in a significant advancement in the research on the microbiota
associated with P. cupana plants (guaraná). Results of investigations carried out by
our group on bacterial diversity associated with leaves (Bogas et al. 2015) and the
rhizosphere of guaraná trees with and without symptoms of anthracnose (Santos
2015), on the evaluation of biotechnological potential of such microorganisms in
the biological control of plant pathogens (Bonatelli et al. 2016), and on the stimula-
tion of plant growth (Batista et al. 2016) evidenced that, in general, symptomatic
leaves displayed a higher number of colony forming units (CFU) of isolated bacte-
ria, and the genera Stenotrophomonas, Pseudomonas, and Pantoea were the most
prevalent. However, in asymptomatic leaves, Acinetobacter and Bacillus were more
frequent. The microorganisms from rhizosphere of healthy guaraná trees showed
higher diversity and richness indexes compared to the rhizosphere of infected guar-
aná tree.
In another study on the diversity of lignocellulotic Agaricomycetes fungi
(Basidiomycota) collected in 12 cities of the state of Amazonas—Brazil 76 species
were identified of which 26 were integrated to the Amazon collection, five to the
national collection and one was recorded as a new species. Moreover, larvicidal
activity assays allowed the identification of Agaricomycetes mycelial extracts with
the potential to eliminate Aedes aegypti (Fonseca 2016). Other examples of micro-
organism variety of natural sources and their applications are presented at Table 5.2.
5.2.1 Microbial Biodiversity in Aquatic Environments
The biodiversity of microorganisms living in watery habitats of Amazonian rivers

has been assessed via independent cultivation methods and with the help of molecu-
lar tools. The Rio Solimões was found to have greater diversity of bacterial genera
than the Rio Negro. The Rio Negro has less bacterial diversity but the finding of
more 16S rRNA gene sequences indicates, for instance, prevalence of some bacterial
genus as the Polynucleobacter, detected by Peixoto et al. (2011). The bacterial
microbiota of the Rio Negro was also characterized by seasonal fluctuations in both
quantitative (colony forming units—CFUs) and qualitative (species identification
Table 5.2 Thesis and publications involving the description of the biodiversity of microorganisms
in the Amazon and their biotechnological potential
Microorgnismsa Approaches References
Chromobacterium
Chromobacterium violaceum Genome Vasconcelos et al. (2003)
Proteolytic potential Cruz Filho et al. (2013)
Proteomic analysis Cordeiro (2009), Cordeiro et al.
(2013), Castro et al. (2015)
Molecular biology Neiva (2005), Dutra (2006),
Listik (2014)
Different isolates Genetic characterization Hungria et al. (2005),
Dall’Agnol et al. 2008)
Other bacteria
Serratia marcescens pigments and antibiotics Santos and Cruz Filho (2011)
Cruz Filho and Teixeira (2013)
Bacillus sp. Alcaline protease Santos and Cruz Filho (2011)
Proteolytic enzymes Teles et al. (2014), Santos and
Cruz Filho (2011)
Proteases Santos and Cruz Filho (2011)
Several species Cellulolytic activities Santos and Cruz Filho (2011)
Endophytic enterobacter Molecular biology Nascimento et al. (2015)
Bacillus thuringiensis Characterization of Souza Filho (2005)
environmental samples
Several species Microbiota in the Negro Neves (2013)
River
Bacteria associated with Diversity and applications Paskinn (2013)
Melipona
Endophytic bacteria Diversity and applications Souza (2016)
Filamentous fungi
Penicillium janthinellum and Xilanolytic fungi Duran et al. (1995)
Aspergillussydowi species
Several species Lignocellulosic and Carvalho et al. (1992), Silva
cellulases activities (2013, 2015), Fernandes (2013)
Larvicidal effects Bucker et al. (2013)
Penicillium and Aspergillus: Pigments and antibiotic (Teixeira et al. 2012a, b)
several spp.
Penicillium spp. Antimicrobian activity (Silva et al. 2010a)
Trichomycetes Diversity and applications Alencar (2003)
Diversity Alencar et al. (2003)
Coletotrichum Lacase production Martinez et al. (2009)
Fungi associated with Diversity Fonseca et al. (2008)
Simuliidae larvae
Yeast
Several isolates Utilize hemicellulosic Cassa-Barbosa (2012),
hydrolyzate Cassa-Barbosa et al. (2015)
Several isolates Amylolitic enzymes Carvalho (1998)
(continued)
Table 5.2 (continued)
Microorgnismsa Approaches References
Several isolates Characterization of Fernandes (2000)
environmental samples
Several isolates Utilize hemicellulosic Matos (2010), Matos et al.
hydrolyzate (2012)
Meyerozyma guilliermondii Ferment d-xylose Matos et al. (2014)
Trichosporon Utilize hemicellulosic Matos et al. (2012)
mycotoxinivorans hydrolyzate
a
Microorganisms from different environments of the Amazon
through 16S rRNA gene analysis) parameters (Neves 2013). The author noted that
the phylum Proteobacteria proved to be dominant and in the ebb period the more
abundant genera were Polynucleobacter, Acinetobacter, and Curvibacter, belonging
to the phylum Proteobacteria. The analysis of microbial biodiversity in lagoons con-
taminated with effluents containing hydrocarbons and the possible impact of xeno-
biotics on the aquatic community of a small stream found in the Amazon forest was
the scope of research carried out by Ruiz (2014).
In an “Igarapé” that bisects the city of Manaus, known as “Igarapé do 40”, bac-
teria were isolated for studies of microbial diversity, potential for bioremediation
and evaluation of antibiotic resistance. Various species of bacteria, including
Chromobacterium violaceum, were found. Besides Gram-negative and Gram-
positive bacteria, other species were found resistant in challenge antibiotics tests.
Isolates with potential for biodegradation of contaminants surfactants were also
identified in stream waters (Manrique 2015).
Using MALDI-TOF technique to identify bacteria and yeasts associated to
Anopheles from samples of aquatic environments researchers found 82 isolates
that have not been previously described within 122 reviews already published
(Souza AQL, personal communication, July; Souza 2016). Other study investi-
gating the same niche through different cultivation methods analyzed genetic
material from 37 samples and obtained 827,842 sequences that were grouped in
6714 OTUS. Nine out of the 20 most frequent OTUS genera were unknown
(Oliveira 2015).
Despite the ecological importance of freshwater fungi, those from the Amazon
are little known. The first study on the decomposition of wood by freshwater
fungi from a lotic environment in the Brazilian Amazon (Cortez 2016; Cortez
et al. 2016) was carried out in a small black water lake. This study showed a
broad diversity of fungi. The authors collected 264 fungi that were distributed in
25 taxa of which 16 were meiosporic ascomycetes and 9 were mitosporic
ascomycetes.
Table 5.3 Classes of bacteria found in 16S rRNA sequencing library and analysis of the RPD II
with number of clones present and their respective percentages
Clones
Cup1 Cup2 Cam2
Class Number (%) Number (%) Number (%)
Acidobacteria 127 40 151 50 106 41
Actinobacteria 13 4 12 4 27 11
Alphaproteobacteria 31 10 31 10 17 7
Anaerolineae 5 2 0 0 2 1
Bacilli 0 0 5 2 1 0
Betaproteobacteria 37 12 24 8 19 7
Clostridia 1 0 0 0 0 0
Cyanobacteria 1 0 1 0 0 0
Deltaproteobacteria 9 3 3 1 10 4
Flavobacteria 0 0 1 0 0 0
Gammaproteobacteria 21 7 17 6 2 1
Gemmatimonadetes 1 0 3 1 1 0
Planctomycetacia 2 1 7 2 0 0
Sphingobacteria 4 1 3 1 4 2
Verrucomicrobiae 13 4 8 3 10 4
Not identified 53 16 36 12 50 20
Total clones 318 302 149
5.2.2 Microbial Diversity in Soils
The microbiota from soil rhizosphere of two cupuaçu plants, Cup1 and Cup2
(T. grandiflorum) and a Camu-Camu plant, Cam2 (Myrciaria dubia) growing in typi-
cal soil of the Amazon, known as acid yellow latosol, was studied by researchers from
INPA using clones from 16S rDNA libraries (Rodrigues 2008). The results of this
study are shown in Table 5.3. Among the 16 phyla identified Acidobacteria was the most
abundant class with 106 clones in Cam2, 127 clones in Cup1, and 151 clones in
Cup2, suggesting that these bacteria are more adapted to acid soils. Bacteria of the
classes Alphaproteobacterias, Betaproteobacterias, Deltaproteobacterias, and
Gammaproteobacterias, all belonging to the phylum Proteobacteria, were also
detected. Proteobacteria constitute the largest taxonomic group of bacteria, and within
the Alphaproteobacteria class, there are bacteria related to important agricultural
activities since they induce the fixation of nitrogen in symbiosis with the plants.
Considering the aspects of economic importance, studies with rhizobia and
phosphate solubilizing bacteria are prioritized, since nitrogen and phosphorus
are the macronutrients with major deficiencies in the Amazonian soils (Oliveira
et al. 1997; Barroso and Oliveira 2001; Chagas et al. 2009a, b, c, 2010b; Hara
and Oliveira 2004, 2005, 2007; Silva et al. 2011). The studies have also been
directed to the production of phytohormones as IAA (indole acetic acid) and
enzymes of economic interest as amylases, proteases, lipases, produced by rhizo-

bia isolates (Oliveira et al. 2006a, b, 2007a, b, 2010a, b; Chagas et al. 2010a;
Prado 2009; Willerding et al. 2011, 2012; Brito 2013).
5.3 Biological Control
The black pod rot of cacao, caused by Phytophthora palmivora, affects cacao crop
worldwide with over 30% of average annual losses. Endophytic fungi from stems
and branches of T. cacao and T. grandiflorum trees growing in the Amazon region
of Brazil, useful for biological control of that severe disease, were investigated by
Hanada and coworkers. Trichoderma martiale was considered a new species of fun-
gus with the potential to control black pod rot of cacao. Besides T. martiale some
other fungi isolates, Pestalotiopsis, Curvularia, Tolypocladium, and Fusarium,
showed high level of activity against the pathogen (Hanada et al. 2008, 2009, 2010).
In a study on ant nests located in the state of Amazonas (Gonzaga et al. 2015;
Freitas et al. 2016), microorganisms associated with cutting ants Atta sexdens were
isolated and identified. Ant colonies with about 5 months of existence, containing all
castes were collected and transferred to the laboratory where monosporic colonies
from the main microorganisms associated with anthills were obtained. They were
identified as Leucoagaricus gongylophorus, T. longibrachiatum, A. flavus, Bionectria
ochroleuca, F. solani, yeasts, Gram-negative, and Gram-positive bacteria.
Leucoagaricus fungi associated with Attini are poorly studied because of the diffi-
culty in isolating and identifying them. Under the conditions occurring in the ant
nests, these microorganisms only develop vegetative structures, the same arising in
laboratory cultures, a fact that complicates the traditional taxonomic identification
of basidiomycetos, based on morphological characteristics. Among the new per-
spectives recently brought to light to perform biological control of ants, the possibil-
ity of controlling the symbiotic microorganisms found in the nest is considered one
of the best alternatives. The use of endophytic bacteria isolated from host plant to
control or eliminate the presence of symbiotic microorganisms present in the ant-
hills was investigated (Gonzaga 2012). Screening assays carried out with 150 endo-
phytic bacteria, coming from 10 plants of the Amazon, revealed that six endophytic
bacteria isolated from Phyllanthus niruri showed promising results and further stud-
ies to identify substances correlated to the exhibited activity are being carried out.
In previously reported studies conducted by Souza et al. (2014, 2015), 122 endo-
phytic bacteria were isolated from cultivars of Musa spp. from the state of Amazonas.
Four bacteria strains were selected because they exhibited antagonistic activities
against Fusariumoxysporum f. sp. cubense and Colletotrichumguaranicola, within
the range 19–30% and 27–35%, respectively. Phylogenetic analysis of the 16S
rDNA regions of these bacteria showed that they are phylogenetically related to
three different species of Bacillus: B. amyloliquefaciens, B. subtilis subsp. subtilis,
and B. thuringiensis.
5.4 B
iological Assays with Natural Products
from Endophytic Fungi
Endophytic fungi isolated from tissue fragments (leaf, twig, stem, and root) of G.
elliptica were classified as Fusarium, Xylaria, Pestalotiopsis, Penicillium,
Cephalosporium, Aspergillus, Colletotrichum (Glomerella), Nectria, and other four
unknown Ascomycetos. Chemical studies of fungal extracts monitored by bioassay
resulted in identification through 1D and 2D NMR analysis and mass spectrometry
of several constituents: a mixture of piliformic acid and 5-carboxylmellein from X.
adscendens; ergosterol peroxide in the endo- and exo-forms; a mixture of bisorbi-
cilinoids: trichodimerol, dihidrotrichodimerol tetrahidrotrichodimerol, and sterig-
matocystin (STC); a mixture of fat acids of P. chrysogenum; a mixture of phenylacetic
acid and 4-methoxyphenylacetic from Aspergillus sp.; fusaric acid and phenylacetic
acid from N. setofusariae. Cytotoxic assays of extracts, fractions, and pure com-
pounds showed high cytotoxic potential against three tumor cell lines for a fraction
of N. setofusariae and STC from P. chrysogenum. This was the first study of G.
eliiptica endophytic fungi collected in the Brazilian Amazon. The discovery of a
strain of P. chrysogenum producing STC and also molecules of the important class
of bisorbicilinoids, reported for the first time in fungal studies conducted in Brazil,
reflects the effectiveness of the strategies adopted for the exploration of microorgan-
isms with potential innovative activities of biotechnological interest (Almeida
2014).
Souza (2001) isolated from the Amazon poisonous plants P. longiflora
(Rubiaceae) and S. cogens (Loganiaceae) 571 endophytic fungi and 74 endophytic
bacteria. P. longiflora and other species of this genus are related to 90% of livestock
deaths in the Amazon region. S. cogens and other species of Strychnos are used by
the natives in the making of “curare” mixture of poisonous compounds. Among the
endophytes isolates of P. longiflora were fungi: Colletotrichum sp. and its telemorfo
Glomerella sp., Guignardia sp., Aspergillusniger, Phomopsis sp., and Xylaria sp.,
addition Burkholderia gladioli a nitrogen fixing bacteria. Isolates of endophytic
fungi from S. cogens were identified as: Colletotrichum sp., Guignardia sp.,
Aspergillus niger, and Trichoderma sp. Extracellular metabolites produced by indi-
vidual cultures of 79 fungi isolated from those plant hosts were tested against patho-
genic and phytopathogenic microorganisms: 19 isolates inhibited one or more
targets. Eight isolates with the best inhibition results showed bioactive molecules
lower than 12,000 Dalton (Souza 2001; Souza et al. 2004).
5.5 Water Bioremediation
Research addressing processes involving bioremediation are strategic to the Amazon

where viable alternatives to remedy or mitigate any possible impacts on the ecosystems
become necessary and urgent. The potential with microorganism bioprospecting to
degrade environmental pollutants constitutes a major tool of bioremediation. One of

the environmental impacts in need of continuous monitoring is related to oil activity
and the Amazon ecosystems are also susceptible to these impacts. The city of Urucu,
located 650 km southwest from the state capital city of Manaus, has the largest oil-
producing land in Brazil. The oil and gas from Urucu field are transported through
the forest by pipeline or inside barrels on ferryboats that navigate the rivers of the
Amazon. In the Amazon region, the floodplain and river environments are highly
under the risk of pollution hazards. They are natural accumulators of pollutant
wastes. The potential risk of accidents with oil and their derivatives is increased by
the use of those waters by local people for domestic uses.
Assays on bioremediation of environments impacted by hydrocarbons employ-
ing microorganisms isolated from aquatic plants, port waters, and hosts as medici-
nal plants have also been conducted by researchers working in the state of Amazonas
(Batista 2009; Araujo 2014; Elias 2013; Santos 2015; Souza Neto 2015; Castro
2015; Santos et al. 2015; Souza 2012a, b). Biosurfactants are very useful in the
biodegradation process of petroleum hydrocarbon. These molecules have attracted
much commerce interest due to lower cost and higher efficiency compared to syn-
thetic surfactants. Souza (2012a, b) tested the potential of bacteria strains isolated
from the macrophyte E. crassipes living in contaminated water in the ports of
Manaus and also endophytic bacteria from medicinal plants for the production of
biosurfactants by evaluating their emulsification activity. The strains that exhibited
the best activity results were Stenotrophomonas sp., Klebsiella sp., Enterobacter
sp., Methylobacterium radiotolerans, and A. baumannii, isolated from E. crassipes;
Candida tropicalis from contaminated port water; P. aeruginosa and S. marcescens
isolated from medicinal plants. Elias (2013) investigated the ability of fungi and a
consortium between fungi and bacteria to degrade petroleum derivatives. The results
were further reinforced by the findings of Araujo (2014) in biodegradation assays
with naphthalene and phenanthrene.
Manrique (2015) isolated 87 bacteria strains from aquatic environments impacted
by domestic and industrial sewage. The microorganisms were aggregated into 12
groups and evaluated by their ability to clean industrial surfactants that were the
main contaminants of that environment. A consortium of the top four strains took 9
days to degrade the surfactants.
As part of a joint work plan carried out by students from the graduate programs
in Biotechnology—UFAM, Master in Biotechnology—UEA, and Biodiversity
Network and Biotechnology of the Amazon—PPG-Bionorte, different Amazonian
environments have been assessed as sources of microorganisms valuable for the
development of biotechnological products and processes. Among the findings there
is the Bacillus anthracis strain that was isolated from the banks of the Amazon
River. This strain is capable of producing a restriction enzyme called BanAI that is
an isoschizomer of the prototype restriction endonuclease Hae III. That was the first
report of a type II restriction endonuclease identified, purified from a natural isolate
of B. anthracis (Chies et al. 2002). Another example is the discovery of a B. pumilus
strain, which was isolated and identified from water samples collected from a small
affluent of the Amazon River. This bacterium produces an enzyme with type II
Table 5.4 Populations of amylolytic, cellulolytic, proteolytic, and ureolytic bacteria in soils of
deposits and natural forest in the region of Urucu (Adapted from Prado 2009)
Amylolytic Cellulolytic Proteolytic Ureolytic
bacteria bacteria bacteria bacteria
Soils 103. g−1 of soil
Native Forest 05 3.3 257 300 97
Deposit 05 14.0 21 11 457
Native Forest 01 0.7 223 53 40
Deposit 01 14.3 19 15 2626
restriction. It is apparently a neoschizomer of the enzyme prototype SacI and was

named Bpu AmI. This was the first report of an isoschizomer and/or neoschizomer
of the prototype SacI identified in the genus Bacillus (Chies et al. 2006).
5.6 Soil Remediation
The role of bacteria carrying oil degrading enzymes or their derivatives has also
been evaluated in Amazon soils (Mari 2008; Lima 2010; Brito 2013). Certain
enzymes may be biological indicators of the recovery of previously forested areas
and presently used for some economic activity as shown in Table 5.4. The data show
that the soils in both deposits had higher amylolytic and ureolytic bacterial popula-
tions when compared with their adjacent forest soils. Moreover, the adjacent forests
had higher populations of cellulolytic and proteolytic bacteria.
This information can be useful when the aim is to restore or rehabilitate degraded
or altered areas, as this process evolves only when populations of plants and micro-
organisms are similar to adjacent forests.
Another research focus has been on the microbiota of a soil type known as
Amazonian Dark Earths (ADE). Most croplands in the Amazon region are acidic,
with low capacity of cationic exchange and low fertility, becoming a limiting factor
for the productivity and sustainability of agricultural production systems of the
region. However, the Amazon region also presents another outstandingly fertile soil
known as “Terra Preta de Indio” (Amazonian Dark Earths or Indian Black Earth).
This black earth can also be found in other countries in South America. The ADE
occurs in archaeological sites in the Amazon region where human action has
enriched these soils with nutrients, probably for the management of organic waste
and fire the pre-Colombian population. The presence of stable organic material and
high biological activity in ADE indicates that this type of soil can be of high microbial
diversity. The modern molecular techniques have allowed part of this diversity to be
exploited (Silva 2009). An example is the study on the catabolic gene diversity for
the bacterial degradation of aromatic hydrocarbons in anthropogenic Amazonian
Dark Earth (ADE) (Germano et al. 2012) and bacterial community structure phb
gene composition and abundance using T-RFLP 454-pyrosequencing and quantitative
PCR essays, respectively (Brossi et al. 2014). Lucheta et al. (2016) compared the
fungal community composition and diversity in Amazonian Dark Earth (ADE) and
the respective nonanthropogenic origin adjacent (ADJ) soils from four different sites
in Central Brazilian Amazon using pyrosequencing of 18S rRNA gene. The most
abundant operational taxonomic units (OTUs) in ADE showed similarities with the
entomopathogenic fungus Cordyceps confragosa and the saprobes Fomitopsis pini-
cola, Acremonium vitellinum, and Mortierella sp. The authors concluded that those
results opened new perspectives for entomopathogenic fungi studies. Functional
screening a metagenomic library from samples of the Amazonian Dark Earths
showed clones encoding a new esterase. Moreover, a gene was identified that showed
similarity with a conserved domain of the β-ketoadipate enol-lactone hydrolase
enzyme participating in the regulation of β-ketoadipate pathway for the degradation
of aromatic esters (Carvalho 2015).
5.7 Microbial Chemistry
From the huge diversity of microorganisms spread over all Amazon environments,
it can be expected a lot more variety of microbial metabolites. It is hardly a world
not explored. Here we present a sample of the studies made by the few regional
groups exploring metabolites produced by bacteria and fungi from plants and other
Amazonian sources. On an unprecedented study with endophytic bacteria, 50 strains
from different Amazon plants were cultivated in triplicate and their metabolites
released into the culture media were submitted to direct injection ESI-ITMS analysis.
According to the MS/MS fragmentation analysis, 25 strains were found to produce
lipopeptides, and eight of their extracts revealed C11–C18 surfactin homologs,
including three (C11, C17, and C18) not yet reported in the literature (Figs. 5.1 and 5.2)
(Mesquita 2015). Surfactins, one of the most important biosurfactants, are a class of
lipopeptides consisting typically in a peptidic ring of seven amino acids attached to
a β-hydroxylated fatty acid containing a chain of 12–15 carbon atoms. These acids
can exist as diverse homologs and isomers, being the most common the C15
3-hydroxy-13-methyl-tetradecanoic acid.
The vast majority of reports on fungi chemistry of endophytic species, carried
out by Amazonian researches, are from the twenty-first century, when some groups
with such interest started their investigations. Here we present a survey on their
efforts to disclose some of the presumable innumerous metabolites that Amazonian
endophytic fungi can produce. All metabolite structures are presented (Table 5.5).
As an example, Trichoderma koningii endophytic fungus, from Strychnos cogens, a
species growing in Manaus (AM, Brazil), produces koninginins A, D, E, and F
(1–4). Pharmacological assays showed that three and four as well vitamin E, exhib-
ited significant inhibition of edema-inducing and myotoxic activities induced by
total venom of Bothrops jararacussu snake and against isolated venom gland toxin
phospholipases A2 (bjPLA2—group IIB) and human secreted PLA2 protein fusion
(hsPLA2—group IIA) (Souza 2005; Souza et al. 2008).
Fig. 5.1 Typical negative ESI-ITMS mass spectrum of surfactin homologs produced by eight
endophytic bacteria from Amazonas state. In highlight, a C15-surfactin structure corresponding to
the peak at m/z 1034 ([M-H]−)
Fig. 5.2 Positive ESI-ITMS mass spectrum of the sodium adduct ion at m/z 1058 ([M + Na]+)of
the C15-surfactin. Fragments are useful to identify the surfactin structure
Screening of aquatic and medicinal plants as hosts of endophytic fungi that could
be the source of novel bioactive metabolites allowed the isolation of more than a
thousand fungus species from the plants Victoria amazonica, Mauritia flexuosa,
Strychnos cf. toxifera, Duguetia stelechantha, Rollinia sp., Piper peltatum,
Peperomia pellucida, and Gustavia sp. From the giant aquatic plant Victoria amazo-
nica, susceptible to attack by aquatic microorganisms such as oomycetes, seven
endophytic fungi showed high activity against Penicillium avelanni and an oomycete
Pythium strain, besides cytotoxic activity against tumoral human cell lines HCT-8
Table 5.5 Structure of metabolites produced by Amazonian fungi
Host, fungus, activities Metabolites
S. Cogens, Trichoderma OH
H R
1
O
koningii, Kon. E and F: venom 3
R
of Bothrops jararacussu, H
H
bjPLA2, and hsPLA2 (Souza O
O
2005; Souza et al. 2008) O OH 2
H OH R
Koninginin A – 1 Koninginin:

D: R1 = OH, R2 = OH, R3 = H – 2
E: R1 = H, R2 = OH, R3 = H – 3
F: R1 = OH, R2 = H, R3 = OH – 4
V. amazonica, Penicillium sp.,
extracts: antitumoral – HCT-8
(colon), MDA-MB 435
(breast), and HL-60 (leukemia)
(Bianco 2010) O
Ergosta-4,6,8(14),22-tetraen-3-one – 5
O
O O O O
O
O
Cordyanidride A methyl ester – 6
O O
O O OH
O O
O O
OH O O
O O
Blennolide H – 7
M. flexuosa, Penicillium sp., OH
Glandicoline B: S. aureus,
Micrococcus luteus, and E. O
coli (Koolen et al. 2012a) N
N N
HO H
O
N 7
NH HO
Glandicoline B – 8 Ergosterol: Δ7 – 9

Brassicasterol: 7,8 dihydro – 10
HO
HO O OH
O OH
Ergosterol peroxide – 11 Cerevisterol – 12

OH
OH OH HO
O
HO
OH HO O
OH OHOH
Mannitol – 13 1-O-α-D-glucopyranoside – 14
(continued)
S.toxifera, Gliocladium sp., H
N O
extract: antitumoral –
MDA-MB435 (breast), HCT-8
(colon), and SF-295 O O N
H
(glioblastoma); 15: M. luteus
Cyclo-(glycyl-L-tyrosyl)-4,4-dimethylallyl ether – 15
(Koolen et al. 2012b)
Citric acid – 16
O OH O
HO OH
HO O
Other metabolites: Steroids 9, 11, and 12

S. toxifera, P. chrysogenum O
O
OH OH
OH O
(Koolen et al. 2014)
O
HO O
O OCH3 O

Kojic acid – 17 Penicillic acid – 18 Patulin – 19
HO O
OH
OH
Cinnamic acid – 20 p-Hydroxybenzoic acid – 21
Other metabolites: Steroids 9, 10, 11, and 12
D. stelechantha, Talaromyces OH O OH
sp.: extract: antitumoral –
MDA-MB435 (breast), HCT-8 O MeO O
(colon), and SF-295 OH O
(glioblastoma) O O OH
(Souza 2012a, b) O OMe
O
HO
OH OH O OH
Austdiol – 22 Dimer of the secalonic acid – 23

D. stelechantha, P. Cl Cl
sclerotiorum, extract: B. cereus O O
(Souza 2012a, b)
N N
O H O OH
O O
O O

Sclerotioramine – 24 Isochromophilone VI – 25
Other metabolite: Steroid 9
(continued)
Rollinia sp., Talaromyces sp. O O O
(Souza 2012)
O
O
O
O
O O
HO
O
Cordyanhydride B – 26
HO
OH O
6,8-dihydroxy-3-methyl-isocoumarin – 27
O O
O O OH
O O
O O
OH O O
O O
Paecilin B – 28
P. peltatum, Talaromyces sp. Only austdiol – 22
(Marcon 2013)
Po. peltatum and Pe. pellucida, O
OH
Xylaria spp. (Marcon 2013) O O
O
O O OH O O OH
N O N O
H H
19,20-epoxy-Cytochalasin Q – 29 Cytochalasin D – 30

OH O
OMe O OMe
O
O
MeO O
MeO O
7-dechloro griseofulvin – 31 5-methoxycarbonyl-mellein – 32

Gustavia sp., X. adscendens OH O
OH
(Almeida 2014)
O
O
HO
O HO O
Piliformic acid – 33 5-carboxymellein – 34
Gustavia sp., N. setofusariae OH
(Almeida 2014) N OH
O
O
Fusaric acid – 35 Phenylacetic acid – 36
(continued)
Gustavia sp., Aspergillus sp. MeO
OH
(Almeida 2014)
O
4-methoxyphenylacetic3 acid – 37
Other metabolite: 36.
Gustavia sp., P. chrysogenum O HO O
OH
(Almeida 2014) O
8'
O O
O OH
O
OH O OMe 8
OH
Sterigmatocistin – 38 Trichodimerol: Δ8 and Δ8′ – 39

Dihydrotrichodimerol: Δ8 or Δ8′ – 40
Tetrahydrotrichodimerol: Neither Δ8 nor Δ8′ – 41
Other metabolites: 11 (in the endo and exo forms)
V. michelii, P. guepinii, HO
OMe O
Chloroisosulo-chrin: S. aureus;
Pestheic acid: antitumoral – OH
PG100 (stomach) (Oliveira
MeO O
et al. 2011; Sousa et al. 2013)
O
Guepinone – 42
OH O OH
R
MeO HO
O OMe
Isosulochrin: R = H – 43 Chloroisosulochrin: R = Cl – 44

O OH
OH
Cl O OH
MeO
OMe
O
Pestheic acid – 45
(continued)
B. guianensis, Pestalotiopsis OH O
O
sp. (Souza et al. 2016)
NH
N O
OH H
(4S)-4,8-dihydroxy-1- Uracil – 47 Uridin – 48
O
NH
HO OH OH
N O
O
OH
HO
OH OH OH OH
Tetralone – 46 Ducitol – 49
Other metabolites: 9, 11, 12, and 21
O
B. guianensis, Aspergillus sp., O
Fumigaclavin C and Pseurotin
A: antibacterial; Mevalolactone, N O
OH
monomethylsulochrin, and O NH
trypacidin A: E. coli, P.
N
aeruginosa, B. subtilis, H
OH
OH
O
O OMe
and S. aureus (Pinheiro et al.
2013a, b) Fumigaclavin C – 50 Pseurotin A – 51
H O OMe
O O O
O
HO OH
OMe OMe
Mevalolactone – 52 Monomethylsulochrin – 53
O OMe
OMe O
O
O
MeO
Trypacidin A – 54
Other metabolites: 9 and 11.
(continued)
B. guianensis, E. rostratum, O
O
Monocerin and annularin I and
MeO O
J: E. coli, P. aeruginosa, and
B. subtilis (Pinheiro et al. O O
2016) MeO
OH O R
Monocerin – 55 Annularin I: R = H – 56
Annularin J: R = OH – 57
Other metabolite: 11
Amazon soil, P. sclerotiorum Cl
(Celestino et al. 2014) O
O
O
O
O
Sclerotiorin – 58
(colon), MDA-MB 435 (breast), and HL-60 (leukemia). One of them, a Penicillium
sp., produced the ergosta-4,6,8(14),22-tetraen-3-one (5), cordyanidride A methyl
ester (6), and blennolide H (7) (Bianco 2010). Mycelial extracts of an endophytic
fungus Penicillium sp., isolated from roots of M. flexuosa, exhibited antimicrobial
activity against S. aureus. The major component of this extract, glandicoline B (8),
also showed activities against S. aureus as well as against Micrococcus luteus and
E. coli. Other compounds obtained from the same extract were ergosterol (9), bras-
sicasterol (10), ergosterol peroxide (11), cerevisterol (12), mannitol (13), and
1-O-α-D-glucopyranoside (14) (Koolen et al. 2012a).
Strychnos cf. toxifera is an alkaloid-containing poisonous plant used by the
Amazon Indians in the manufacture of curare poison. Ethyl acetate extracts of the
liquid culture (ISP2 medium) of Gliocladium sp., isolated from S. toxifera, showed
potent activity against cell lines of human breast cancer (MDA-MB435), human
colorectal cancer (HCT-8), and human glioblastoma cancer (SF-295). The same
extract afforded a huge amount of the diketopiperazine alkaloid cyclo-(glycyl-L-
tyrosyl)-4,4-dimethylallyl ether (15), which exhibited antimicrobial activity against
M. luteus at the concentration of 43.4 mM. This molecule is a precursor of gliotoxin-
derived alkaloids, which are related to immunosuppressive, antibacterial, antifun-
gal, and antiviral activities. Other substances obtained from the same Gliocladium
sp. strain were citric acid (16) and the steroids 9, 11, and 12 (Koolen et al. 2012b).
The mycelia MeOH extract of Penicillium chrysogenum, another endophytic fungus
from the trunk of the same plant, produced the mycotoxins kojic acid (17), penicillic
acid (18), and patulin (19), along with cinnamic acid (20), p-hydroxybenzoic acid
(21), and the steroids 9–12 (Koolen et al. 2014).
Annonaceae species are well known to produce alkaloids. Endophytes from
Annonaceae plants were assayed against microorganisms and tumor cell lines and
some of those microorganisms were further investigated through chemical studies.

Talaromyces sp. DgCr22.1b colonizing Duguetia stelechantha (active at 90%
against human tumor cell lines HCT-8—colon, MDA-MB 435—breast, and
SF-295—glioblastoma) produced austdiol (22) and the 4,4′-linked secalonic acid
dimer (23) while P. sclerotiorum DgC32.2 (powerful against Bacillus cereus) pro-
duced besides 9, the azaphilone dyes sclerotioramine (24) and isochromophilone VI
(25). Talaromyces sp. AnspCr11.1 (active against Penicillium avelani) from Rollinia
sp., produced cordyanhydride B (26), 6,8-dihydroxy-3-methyl-isocoumarin (27),
and paecilin B (28) (Souza 2012a, b).
Endophytic fungi isolated from shrubby species also have been showed as
sources of important metabolites as 22, produced by Talaromyces sp. from P. pelta-
tum, and 19,20-epoxy-cytochalasin Q (29), cytochalasin D (30), 7-dechloro griseo-
fulvin (31), and 5-methoxycarbonyl-mellein (32), produced by Xylaria spp. from P.
peltatum and P. pellucida (Marcon 2013). Moreover, four fungal strains from the
woody Gustavia sp. were selected to isolate bioactive metabolites, resulting in a
mixture of piliformic acid (33) and 5-carboxymellein (34) from Xylaria adscen-
dens, fusaric, and phenylacetic acids (35–36) from Nectria setofusariae, a mixture
of 36 and 4-methoxyphenylacetic acid (37) from Aspergillus sp., and 11 in the endo
and exo forms, sterigmatocistin (STC) (38), as well as a mixture of the bisorbicil-
linoids trichodimerol (39), dihydrotrichodimerol (40), and tetrahydrotrichodimerol
(41), plus a mixture of fatty acids from Penicillium chrysogenum (Almeida 2014).
Fungus studies of other researchers can be represented by investigation of endo-
phytes from Virola michelii and Bahuinia guianensis, plants used by Amazonia
populations for treatment of skin rashes caused by fungi and to combat infectious
and renal diseases, respectively.An endophytic fungus strain of Pestalotiopsisguepinii
from V. michelii produced a new anthraquinone derivative named guepinone (42)
together to isosulochrin (43) and chloroisosulochrin (44), which was active against
Staphylococcus aureus (Oliveira et al. 2011). The same fungus produced pestheic
acid or dihydromaldoxin (45), a chlorinated diphenylic ether that demonstrated
low cytotoxic effect against a gastric adenocarcinoma cell line (PG100) (Sousa
et al. 2013).
Eight compounds were produced by Pestalotiopsis sp. EJC07, an endophytic
fungus strain from B. guianensis: 9, 11, 12, 21, (4S)-4,8-dihydroxy-1-tetralone (46),
uracil (47), uridin (48), and ducitol (49) (Souza et al. 2016). As a possible relation-
ship with the vegetal anti-infective activity, the endophytic fungus Aspergillus sp.
EJC08 produced two broad-spectrum antibacterial alkaloids known as fumigaclavin
C (50) and pseurotin A (51). Other substances produced by the strain EJC08 were 9,
11, mevalolactone (52), monomethylsulochrin (53) and trypacidin A (54), with
good antimicrobial activity against Escherichia coli, Pseudomonas aeruginosa,
Bacillus subtilis, and Staphylococcus aureus (Pinheiro et al. 2013a, b). Exserohilum
rostratum, also an endophyte from Bauhinia guianensis, produced together with 11,
Monocerin (55) and the annularin I (56) and annularin J (57), compounds with mod-
erate activity against Escherichia coli, Pseudomonas aeruginosa, and Bacillus sub-
tilis (Pinheiro et al. 2016).
In a search to isolate the Amazon soil fungi able to synthesize pigments, five
strains cultured on Czapeck broth were detected and further identified as Penicillium
sclerotiorum 2AV2, P. sclerotiorum 2AV6, Aspergilluscalidoustus 4BV13, P. citri-
num 2AV18, and P. purpurogenum 2BV41. The pigment sclerotiorin (58) from P.
sclerotiorum 2AV2 was identified. Exogenous addition of rhamnose or peptone to
the culture medium enhanced the yields of sclerotiorin (Celestino et al. 2014).
Brazil has achieved great advancements in the area of science and technology
and in the Amazon there were also improvements in science, though there are still
some obstacles to overcome. Two motives have been obstructing the identification
and the sustainable use of microbial biodiversity in the Amazon. The first regards
the small number of research institutions in the north of the country and in conse-
quence a reduced number of active researchers in those institutions. The second
reason constitutes one of the biggest challenges for sustainable economic produc-
tion in the Amazon that is the need to revise the basis of production primarily incor-
porating innovative biotechnological processes effective for supporting a new
development matrix. Considering that a vast diversity of new species of fungus
already described were from tropical countries, the exploitation of the Amazon
microbiological diversity is of prime importance.
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Chapter 5

Overview on Biodiversity, Chemistry,

Jose Odair Pereira, Antonia Queiroz Lima de Souza, Afonso Duarte Leão de

J.O. Pereira (*)

© Springer International Publishing AG 2017 71

Keywords Amazonian rainforest • Endophytic microorganisms • Biorremediation •

Data on biodiversity, reported by The Brazilian Ministry of the Environment—

by the Universidade Federal do Amazonas (UFAM), Universidade do Estado do

5.2 Amazon Biodiversity

In the state of Amazonas, there are important collections of cultures of microorgan-

maintained in that collection. The endophytic microorganisms deposited in this col-

5.2.1 Microbial Biodiversity in Aquatic Environments

The biodiversity of microorganisms living in watery habitats of Amazonian rivers

5.2.2 Microbial Diversity in Soils

enzymes of economic interest as amylases, proteases, lipases, produced by rhizo-

5.3 Biological Control

5.5 Water Bioremediation

Research addressing processes involving bioremediation are strategic to the Amazon

degrade environmental pollutants constitutes a major tool of bioremediation. One of

restriction. It is apparently a neoschizomer of the enzyme prototype SacI and was

5.6 Soil Remediation

5.7 Microbial Chemistry

Koninginin A – 1 Koninginin:

Glandicoline B – 8 Ergosterol: Δ7 – 9

Ergosterol peroxide – 11 Cerevisterol – 12

Other metabolites: Steroids 9, 11, and 12

Austdiol – 22 Dimer of the secalonic acid – 23

19,20-epoxy-Cytochalasin Q – 29 Cytochalasin D – 30

7-dechloro griseofulvin – 31 5-methoxycarbonyl-mellein – 32

Sterigmatocistin – 38 Trichodimerol: Δ8 and Δ8′ – 39

Isosulochrin: R = H – 43 Chloroisosulochrin: R = Cl – 44

some of those microorganisms were further investigated through chemical studies.

Banhos EF (2016) Análises moleculares de linhagens selvagens e mutantes de Pestalotiopsis spp.

Listik AF (2014) Plasmídeos naturais de Chromobacterium violaceum: análise de sequências e

Oliveira MR (2015) Avaliação da Biodiversidade de bactérias não cultiváveis associadas à

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5.2 Amazon Biodiversity

5.2.1 Microbial Biodiversity in Aquatic Environments

5.2.2 Microbial Diversity in Soils

5.3 Biological Control

5.5 Water Bioremediation

5.6 Soil Remediation

5.7 Microbial Chemistry