Microbial communities, processes and functions in acid mine drainage ecosystems 2016

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Microbial communities, processes and functions in acid
mine drainage ecosystems
Lin-xing Chen1, Li-nan Huang1, Celia Méndez-Garcı́a2,
Jia-liang Kuang1, Zheng-shuang Hua1, Jun Liu1 and
Wen-sheng Shu1
Acid mine drainage (AMD) is generated from the oxidative
dissolution of metal sulfides when water and oxygen are
available largely due to human mining activities. This process
can be accelerated by indigenous microorganisms. In the last
several decades, culture-dependent researches have
uncovered and validated the roles of AMD microorganisms in
metal sulfides oxidation and acid generation processes, and
culture-independent studies have largely revealed the diversity
and metabolic potentials and activities of AMD communities,
leading towards a full understanding of the microbial diversity,
functions and interactions in AMD ecosystems. This review
describes the diversity of microorganisms and their functions in
AMD ecosystems, and discusses their biotechnological
applications in biomining and AMD bioremediation according
to their capabilities.
Addresses
1
State Key Laboratory of Biocontrol, Guangdong Key Laboratory of
Plant Resources, College of Ecology and Evolution, Sun Yat-Sen
University, Guangzhou 510275, PR China
2
Carl R. Woese Institute for Genomic Biology, University of Illinois at
Urbana-Champaign, Urbana, USA
Corresponding author: Shu, Wen-sheng ([email protected])
can dramatically accelerate the acid generation process
and therefore play significant roles in material and energy
flows of the whole ecosystem [3,6]. Due to the dominance by a few taxa more than a lack of complexity [7,8]
and its remarkably simple geochemical features [9],
AMD environments have been established as model
systems for quantitative analyses of microbial ecology
and community function [3,4], and as ideal targets
for biogeochemical studies of iron and sulfur cycles [10–12].
Moreover, microorganisms from AMD environments are
the major contributors in biomining of low-grade ores [13],
and have significant potentials in AMD bioremediation
[2]. This review summarizes the taxonomic diversity
and metabolic functions of AMD microorganisms and their
biotechnological applications in biomining and AMD bioremediation.
The diversity of AMD microorganisms
During the last several decades, isolation and cultivation
methods [4,9], and 16S rRNA gene and meta-omics
based molecular analyses [3,7,14], have drastically
enlarged our knowledge of microbial diversity in AMD
ecosystems (Figures 1 and 2).
Current Opinion in Biotechnology 2016, 38:150–158
This review comes from a themed issue on Environmental
biotechnology
Edited by Benardo Gonzalez Ojeda and Regina Wittich
http://dx.doi.org/10.1016/j.copbio.2016.01.013
0958-1669/# 2016 Elsevier Ltd. All rights reserved.
Introduction
Acid mine drainage (AMD) is characterized by low pH
and high concentrations of metals and sulfate, representing an extreme environment to life [1] as well as a major
environmental challenge worldwide [2]. AMD ecosystems include distinct environments of AMD solutions,
sediments, and biofilms [3], providing multiple niches
for AMD microorganisms. The microorganisms thriving
in AMD environments have evolved with distinct mechanisms to the extreme conditions [4,5], by which they
Current Opinion in Biotechnology 2016, 38:150–158
Proteobacteria, Nitrospira, Actinobacteria, Firmicutes, Acidobacteria, Aquificae and Candidate division TM7 represent
the primary bacterial lineages detected (Figure 1). The
most extensively studied taxa are iron- and/or sulfuroxidizing Acidithiobacillus spp. (Acidithiobacillia) [15–17],
and iron-oxidizing Leptospirillum spp. (Nitrospira) [18–20].
The lesser known ‘Ferrovum’ spp. (Betaproteobacteria),
which have been widely detected as dominant members
and suggested as major iron-oxidizing populations in lessrestrictive pH conditions [7,21,22,23], have recently
been obtained in pure culture [24]. The majority members in these three genera are validated as autotrophs
(Figure 2), fixing carbon from open environments. Multiple heterotrophic acidophiles co-occurring with these
carbon-fixers may drive the carbon cycling by consuming
organic carbons, including members from Alphaproteobacteria (Acidiphilium, Acidocella, Acidicaldus, Acidomonas,
Acidisphaera) [25–27], Gammaproteobacteria (Acidibacter ferrireducens and Metallibacterium scheffleri) [28,29], Actinobacteria (Acidithrix ferrooxidans, Ferrimicrobium acidiphilum
and Acidimicrobium ferrooxidans) [6,30], and Acidobacteria
[31,32]. Additionally, Sulfobacillus spp. (Firmicutes) were
detected as mixotrophs [33–35], while Alicyclobacillus spp.
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Microbiology ecology in AMD Chen et al. 151
Figure 1
BetaGa
mm
pH
range
a
illi
Eu
ry
ar
ch
ae
ot
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ba
io
ith
id
Ac
a
a-
Relative abundance (%)
0
20
40
60
80
100
< 2.0
Alpha
2.0-2.4
Crenarch
aeota
2.4-2.6
Acid
oba
c
teria
2.6-2.8
2.8-3.0
> 3.0
De
lta
-
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isio
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Ca rvar
Pa
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io ida
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TM
7
sp
e
ira
tro
Ni
Firm
icute
s
a
acteri
ob
Actin
Current Opinion in Biotechnology
The taxonomic and phylogenetic diversity of frequently detected prokaryotic microorganisms in AMD ecosystems including environments of acid
solutions, biofilms and sediments (left panel), and their distribution in AMD solutions of different pH ranges (right panel) (data from [7]; a total of
125 AMD samples).
(Firmicutes) were documented as heterotrophs or chemolithoautotrophs in mine environments or AMD treatment
plants [2,36]. Some representatives of sulfate-reducing
bacteria (SRB) within Gammaproteobacteria, Deltaproteobacteria and Firmicutes have also been detected, including
members from the genera of Thermodesulfobium, Syntrophobacter, Desulfurella, Desulfomonile, Desulfovibrio and
Desulfosporosinus [37]. Other less frequently detected
bacterial taxa include Gallionella ferruginea and the putative heterotrophic growers Thiomonas spp. [38–41].
Archaea, including the phyla of Euryarchaeota, Crenarchaeota and Candidate division Parvarchaeota, typically
constitute a minor fraction of AMD communities
[3,4,9,14], but have been found dominant in specific mining environments [42–44]. In the Euryarchaeota,
members from the iron-oxidizing and cell wall-lacking
genus Ferroplasma are the most widely detected [42–
45,46,47–50]. Importantly, Ferroplasma spp. have been
found to dominate the later stages of the acidification
processes of mine wastes [43,44], indicating their critical
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roles in AMD generation. Another cell wall-lacking genus
Acidiplasma was also isolated and detected with ironoxidation and reduction activities [51]. Besides, multiple
Thermoplasmatales archaeon genomes (alphabet plasmas)
have been reconstructed from metagenomic datasets, and
one of those (G-plasma) was cultured as Cuniculiplasma
divulgatum to represent a new family Cuniculiplasmataceae
[52]. Within the Crenarchaeota, the iron and/or sulfur
oxidizers from genera Acidianus, Metallosphaera, Stygiolobus, Sulfolobus and Sulfurisphaera have been mostly identified as extreme thermophiles inhabiting AMD
ecosystems [9]. The poorly studied archaeal group
ARMAN (Archaeal Richmond Mine Acidophilic Nanoorganisms) in Candidate division Parvarchaeota was firstly
discovered in the acidophilic biofilms from the Richmond
Mine at Iron Mountain, California [53,54]. Closely related
gene sequences have been recovered in other AMD
environments [42,55], however their ecological roles have
not been clearly revealed, due to their relatively low
activities [23,42,54]. The filterable ARMAN spp. were
initially speculated to be aerobic based on proteomic data
Current Opinion in Biotechnology 2016, 38:150–158
152 Environmental biotechnology
lfu
r
itr
og
ar en
bo
n
C
N
Acidithiobacillus caldus DSM 22753
Acidianus brierleyi DSM 1651
Acidithiobacillus caldus ATCC 51756
Acidiplasma aeolicum DSM 18409
Acidithiobacillus ferrivorans DSM 22755
Acidiplasma cupricumulans DSM 16551
Acidithiobacillus ferrooxidans ATCC 23270
“Ferroplasma acidarmanus” fer1
Acidithiobacillus ferrooxidans ATCC 53993
“Ferroplasma sp. Type II”
Acidithiobacillus thiooxidans DSM 17318
Ferroplasma acidiphilum
Acidithiobacillus ferriphilus DSM 100412
Metallosphaera sedula DSM 535
Acidithiobacillus ferridurans ATCC 33020
Picrophilus torridus DSM 9790
Acidithrix ferrooxidans DSM 28176
Picrophilus oshimae DSM 9789
Acidibacter ferrireducens DSM 27237
Sulfolobus acidocaldarius DSM 639
Acidiphilium cryptum JF-5
Sulfolobus solfataricus P2
Sulfolobus tokodaii JCM10545
Acidiphilium multivorum AIU301
Stygiolobus azoricus DSM 6296
“Ferrovum myxofaciens” P3G
Thermoplasma acidophilum DSM 1728
“Ferrovum” sp. FKB7
Thiomonas delicata DSM 17897
Desulfomonile tiedjei DSM 6799
Desulfovibrio longus DSM 6739
Leptospirillum ferriphilum DSM 17947
Bacteria
Acidiphilium angustum ATCC 35903
Thermoplasma volcanium GSS1
Archaea
O
xi
d
R ati
ed o
n
O ucti
xi on
da
R ti
ed o
u n
Fi ctio
xa n
R tio
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u
Fi ctio
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n
Su
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og
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N
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r
Su
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O ucti
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da
R ti
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Fi ctio
xa n
R tio
ed n
u
Fi ctio
xa n
tio
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Iro
n
Figure 2
Thermogymnomonas acidicola JCM 13583
“Thermoplasmatales archaeon A-plasma”
“Thermoplasmatales archaeon C-plasma”
“Thermoplasmatales archaeon D-plasma”
“Leptospirillum ferrodiazotrophum”
“Thermoplasmatales archaeon E-plasma”
Leptospirillum ferrooxidans ATCC 29047
“Thermoplasmatales archaeon I-plasma”
Leptospirillum group IV UBA BS
Cuniculiplasma divulgatum JCM 30642
“Leptospirillum rubarum”
Candidatus Micrarchaeum acidiphilum ARMAN-2
Alicyclobacillus disulfidooxidans ATCC 51911
Candidatus Parvarchaeum acidiphilum ARMAN-4
Sulfobacillus acidophilus DSM 10332
Candidatus Parvarchaeum acidiphilum ARMAN-5
Sulfobacillus thermosulfidooxidans DSM 9293
Desulfosporosinus sp. aSRB1 (FK)
Desulfosporosinus sp. aSRB2 (FK)
Acidimicrobium ferrooxidans DSM 10331
Experiment confirmed with feature
With genes, while not experiment confirmed
Ferrimicrobium acidiphilum DSM 19497
Acidobacterium capsulatum ATCC 51196
Hydrogenobaculum acidophilum DSM 11251
Metallibacterium scheffleri DSM 24874
Experiment confirmed without feature
No information, or not analyzed
Current Opinion in Biotechnology
The metabolic characteristics of representative prokaryotic microorganisms detected in AMD ecosystems, including their capabilities in the cycling
of iron, sulfur, nitrogen and carbon, which are significant for AMD microorganisms. The information is based on cultivation-dependent approaches
and/or predicted from -omics data.
[54], while later found to exclusively inhabit the anoxic
areas of biofilms by fluorescence in situ hybridization
(FISH) analysis and could only be enriched using anoxic
culturing techniques [56].
The detected eukaryotic microorganisms in AMD environments included Archaeplastida, Stramenophiles, Alveolates, Rhizaria, Excavata, Opisthokonta, and algae and
fungi [57–59]. Although the current knowledge of
AMD eukaryotic microorganisms is still limited, while
their significant roles, including those in the whole ecosystem function and AMD bioremediation, should not be
omitted (see below).
From diversity to ecosystem function:
processes and functional networks
The successful isolation and functional validation of
AMD acidophiles, and the application of approaches
Current Opinion in Biotechnology 2016, 38:150–158
including meta-omics [40,42,46], taxa-specific gene
chips [60,61], FISH [56,62] and DNA-stable isotope
probing (DNA-SIP) [35], have rapidly advanced our
understanding of the microbial roles, distributions and
interactions in AMD ecosystems (Figures 2 and 3).
The oxidation of iron and sulfur is vital for acidophilic
chemolithoautotrophic microbes to gain energy [4]. The
oxidation of Fe2+ to Fe3+ is a process fueled by the oxidative
environment and driven by the activities of a wide array of
indigenous microorganisms, such as members of Leptospirillum, ‘Ferrovum’, Acidithiobacillus, Ferroplasma, Sulfobacillus
and Sulfolobus [4,6,9]. The mechanisms for energy conservation and associated genes in species belonging to this
functional group have been extensively reported [12]. As the
primary oxidant in low pH AMD environments [4],
obtained Fe3+ can oxidize acid-insoluble metal sulfides
(e.g., FeS2, MoS2) to generate thiosulfate, and acid-soluble
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Microbiology ecology in AMD Chen et al. 153
Figure 3
sunlight
darkness
N2
CO2
CO2
N2
Air / water interface
N2
early biofilm
NH4+ (CH2O)n
+
4
NH
Fe3+
S2O32RISC
Fe2+
H+ SO42-
AMD sediment
Leptospirillum spp.
Acidithiobacillus spp.
H2
Fe3+
AMD solution
pH < 4
CO2 N2
mature biofilm
Fe2+
Fe2+
N2 CO2
CO2
S0
(CH2O)n
2
NO
SO32-
NH4+
NO3(CH2O)n
SO42-
FeS2
actinobacteria
Sulfobacillus spp.
(CH2O)n
S2O32- VFA
RISC
S0
NH4+
SO32-
CO2
degrading biofilm
S2Ferrovum spp.
Acidiphilium spp.
archaea
eukaryotes
SRBs
Current Opinion in Biotechnology
Scheme displaying the main element cycling operating in AMD ecosystems in all identifiable environments (acid solution, sediment, and biofilm)
and involved taxa (see legend). Dissolution of pyrite (FeS2) present in the sediments fuels AMD generation. Redox reactions involving iron
dominate in acid solution and at early biofilm stages as compared to mature biofilms. Oxidation of reduced inorganic sulfur compounds (RISCs)
occurs across environments and gains importance in the mature biofilm. Autotrophic carbon and nitrogen fixation take place closer to the
air/water interface and heterotrophs are responsible for biofilm degradation at higher depths, where anaerobic respiration of sulfate occurs,
contributing to generation of RISCs. Degrading biofilm is the biofilm sink to the sediment–solution interface, which degrades under microaerobic
and anaerobic conditions. Colors reflect the elemental nature of the transformations depicted: red, Fe; yellow, sulfur; green, nitrogen; brown,
carbon; blue, hydrogen. Abbreviations: VFA, volatile fatty acid; SRB, sulfate reducing bacteria.
metal sulfides (e.g., FeS, ZnS) to generate elemental sulfur
via intermediary polysulfides [63]. Other reduced inorganic
sulfur compounds (RISCs) such as sulfite and tetrathionate,
may also be generated. These, together with the thiosulfate
and elemental sulfur, can be oxidized to sulfate by sulfuroxidizers with enzymes encoded by multiple genes, which
(and the associated mechanisms) have been reviewed recently [11]. Furthermore, the reduction of sulfate with the
generation of sulfide has been detected in AMD ecosystems
[64], thus completing the sulfur cycle in this extreme
environment. This happens in the mineral-loaded sediments with a massive occurrence of SRBs where organic
carbons are available [33,65], resulting in higher pH and
lower levels of redox potential and dissolved metals. Likewise, Fe3+ is susceptible to biological reduction to Fe2+ by
bacteria (e.g., Acidiphilium spp., Acidithiobacillus spp.) and
archaea (e.g., Ferroplasma spp., Acidiplasma aeolicum) under
anaerobic conditions. Such processes have been documented in both natural settings [29,36] and laboratory conditions
[47,51].
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Organic carbon and nitrogen are limited in AMD ecosystems [4]. Although exogenous inputs of these resources
are possible, the existence of microbial species capable of
carbon and nitrogen fixation coupled with iron and sulfur
oxidation will ensure a steady supply of these elements
into the system [18,23,42,66], indicating a vital role of
these organisms for the growth and maintenance of communities. Notably, the essential function of nitrogen
fixation is executed by a limited number of low abundance taxa [2346], and removal of these keystone
species will likely result in the collapse of the entire
community [18], an important implication for AMD prevention. Also, the acid-tolerance algae and fungi could
provide sufficient low molecular weight organic carbon
resources for the heterotrophs [59], such as SRBs and Fe3+
reducer, thus serve as an important role in completing the
cycling of iron and sulfur in AMD ecosystems.
Acidophilic biofilms represent the most extensively studied environment in AMD ecosystems [3]. These biofilms
Current Opinion in Biotechnology 2016, 38:150–158
154 Environmental biotechnology
can vary substantially in their morphologies due to differences in the environment chemistry, mirroring their
changes at the functional level (Figure 3). Thin subaerial
biofilms floating in AMD solutions rely actively on Fe2+
and RISCs oxidation, especially at early developmental
stages [19,67]. In contrast, thicker and more mature microbial growths possess a more heterotrophic metabolism that
appears related to increasing proportions of Thermoplasmatales archaea [68,69]. A restricted set of microbes, particularly At. ferrooxidans [70,71], Leptospirillum spp. (Group II
and III) [72], and ‘Ferrovum’ spp. [23], have been shown
to contribute to the turnover of extracellular polymeric
substances, therefore contributing to the metabolism of the
ubiquitous carbon source that allows the establishment of a
more heterotrophy-inclined community in time. It has
been suggested that archaea inhabiting mature and degrading AMD biofilms, with strong evidence for Thermoplasmatales and ARMAN, would possess a heterotrophic
metabolism, whereas the aerobic iron-oxidizing Leptospirillum may have a limited anaerobic capacity for the consumption of biofilm carbon [36]. Additionally, mixed acid
fermentation have also been proposed to take place in
biofilms [31,61], the excreted acetate from the fermentation process could serve as an electron donor for the
heterotrophic SRBs and Fe3+ reducers, and may also
negatively affect the growth of chemolithotrophic microorganisms (e.g., Acidithiobacillus spp., Leptospirillum spp.)
through iron and sulfur oxidation inhibiting [73].
AMD acidophiles also have evolved with multiple mechanisms for adaptation of the high metal concentrations,
including converting them into less toxic forms (through
precipitation, oxidation, or reduction), or pumping them
into the periplasm or out of the cells [74]. Besides, the
fungi in AMD ecosystems are capable to absorb heavy
metals into their cells or onto the extracellular polysaccharide [59], thus reducing the solubility of heavy metals,
which is benefit for the growth of other indigenous
microorganisms.
Biotechnological applications of AMD
microorganisms
The knowledge about microorganisms in AMD ecosystems, as summarized above, provides the basic clues for
Figure 4
Model reactor
Air Fe oxidizers
Module 1
AMD (pH=2.23)
High levels of Fe2+,
Fe3+,Zn2+,Mn2+,
Cu2+,SO42-
Fe2+ → Fe3+
NaOH
NaOH
Module 2
Fe3+ ↓
Module 3
[Fe8O8(OH)6(SO4)]
In
[Fe8O8(OH)6(SO4)]
(CH2O)n
N2 SRBs
CO2
H2S
1. Raise pH
2. Recover metals
Fe3+ ↓
Effluent (pH=8.10)
Low levels of Fe2+,
Fe3+,Zn2+,Mn2+,
Cu2+,SO42-
H2S
Biofilm
Module 5
Module 4
MnS ↓
CuS↓ ZnS ↓
Out
Current Opinion in Biotechnology
Schematic representation of an integrated reactor system for AMD bioremediation using AMD-related microorganisms, including sections for pH
adjustment and heavy metals recovery. The specific role of modules are as follows: module 1, Fe2+ in the AMD solutions is oxidized to Fe3+ by
iron oxidizers with the input of air; module 2 and module 3, two sequential modules for sufficient precipitation of Fe3+ as schwertmannite; module
4 and module 5, SRBs feeding with organic carbon resources reduce sulfate to generate H2S, which is used for the precipitation of Cu2+, Zn2+,
Mn2+. Please note that the excess H2S should be absorbed from into the air.
Current Opinion in Biotechnology 2016, 38:150–158
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Microbiology ecology in AMD Chen et al. 155
their biotechnological applications in biomining and
AMD bioremediation.
Biomining refers to the extraction of metals from sulfidic
ores and concentrates using the capacities of acidophilic
chemolithotrophic microorganisms in accelerating the
oxidative dissolution of sulfide minerals [13], and has
been reviewed recently [75]. As the most widely applied
biomining operation, heap leaching is mediated by microbial consortia of acidophiles, including Fe2+ oxidizing
autotrophs, H2SO4 generating autotrophs, and also heterotrophs and mixotrophs [13,75].
Integrated reactor systems based on the activities of ironoxidizers and SRBs have recently been used to lower the
levels of acidity and to recover heavy metals in AMD
solutions (e.g., [76]). In an unpublished work by Liu
et al., AMD from DaBaoShan polymetallic ore of Guangdong, China [42], was conducted for bioremediation using
an integrated reactor systems. As illustrated in Figure 4,
influent Fe2+ is firstly oxidized to Fe3+ and then precipitated as schwertmannite with the input of alkaline materials (e.g., NaOH). Next, sulfate is reduced by the SRBs
inhabiting the artificial biofilms in the system, and H2S
generated is used for the precipitation of Cu2+, Zn2+ and
Mn2+ as metal sulfides.
In general, while biomining takes full advantage of ironand sulfur-oxidizers to the extreme [13,75], the activities
of sulfate reducers are vital in the AMD bioremediation
systems [2,76]. It should be noted that, in both biomining operations and bioremediation systems, the microbial communities vary between different sections,
with clearly defined and specific roles for the populated
microorganisms. Furthermore, in any single biological
unit, a microbial consortium with similar features, not a
single taxon, is responsible for the system functions [75].
The microbial consortium for a specific function in the
system, may comprise several taxa [75], and/or different
genotypes of a single taxa as speculated from natural
AMD ecosystems [3], with differences in metabolic
potentials, likely due to the multiple micro-niches generated.
Biomining has been well established and widely applied
[75], while it is not the case for AMD bioremediation
technique using AMD indigenous microorganisms [76].
Though many attempts have been performed for AMD
bioremediation, and at least two commercial processes
have been documented successful (see [2] for details),
however, more environmentally benign and economical
options are needed. As a potential AMD bioremediation
operation, integrated bioreactor systems have been demonstrated to remediate the test AMD solutions with high
performance (Figure 4; [76], unpublished data Liu et al.),
however, further efforts, including in-depth investigations of the microbial processes therein and isolation of
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naturally occurring acidophilic SRBs and construction of
efficient artificial consortia, are needed to address the
multiple challenges towards their full-scale applications.
Conclusions
Engineered biological systems mirror in many ways the
interactions and processes of large-scale ecosystems [77].
The development of molecular approaches and their wide
applications in the studies of natural AMD communities
have resulted in remarkable insights into the diversity and
function of these extraordinary organisms and have provided significant clues for biotechnological applications of
AMD microorganisms. Meanwhile, recent high throughput sequencing-based investigations have detected a
large number of rare taxa in acidic environments [7,8].
These low abundance species may play a crucial role in
functional stability over time and upon perturbations.
Future extensive meta-omics and single cell genomics
will provide novel insights into these lesser-known, but
potentially important taxa in AMD communities. Additionally, the complex ecological interactions between
different taxa including viruses, prokaryotes, eukaryotic
microbes, deserve more attention. On the other hand, the
reductive processes in AMD ecosystems (including those
of sulfur and iron cycling), as well as the community
diversity and dynamics of the associated microorganisms,
which are particularly crucial for AMD bioremediation,
merit further studies. Ultimately, an ecologically sound
and efficient use of AMD microbes will benefit from a
thorough knowledge of the ecology of all community
members populating AMD ecosystems.
Acknowledgements
We thank the three anonymous reviewers for their valuable comments on
the manuscript. This work was supported by the National Natural Science
Foundation of China (U1201233, U1501232, 31370154), the Guangdong
Province Key Laboratory of Computational Science and the Guangdong
Province Computational Science Innovative Research Team.
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