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

Available online at www.sciencedirect.com
ScienceDirect
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 (shuws@mail.sysu.edu.cn)
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.
www.sciencedirect.com
Microbiology ecology in AMD Chen et al. 151
Figure 1
BetaGa
mm
pH
range
a
illi
Eu
ry
ar
ch
ae
ot
c
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
-
n
isio
div
te ota
a
d
e
i
nd cha
Ca rvar
Pa
e
ica
uif
Aq C
di an
vis d
io ida
n te
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
www.sciencedirect.com
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
ed n
u
Fi ctio
xa n
tio
n
Su
Iro
n
itr
og
ar en
bo
n
C
N
lfu
r
Su
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
ed n
u
Fi ctio
xa n
tio
n
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
www.sciencedirect.com
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].
www.sciencedirect.com
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
www.sciencedirect.com
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
www.sciencedirect.com
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.
References and recommended reading
Papers of particular interest, published within the period of review,
have been highlighted as:
of special interest
of outstanding interest
1.
Rothschild LJ, Mancinelli RL: Life in extreme environments.
Nature 2001, 409:1092-1101.
2. Johnson DB, Hallberg KB: Acid mine drainage remediation
options: a review. Sci Tot Environ 2005, 338:3-14.
An overview of AMD remediation approaches, including those involving
with indigenous AMD microorganisms.
3.
Denef VJ, Mueller RS, Banfield JF: AMD biofilms: using model
communities to study microbial evolution and ecological
complexity in nature. ISME J 2010, 4:599-610.
A review of using AMD biofilm as a model system for microbial and
ecological studies, including descriptions of meta-omics methodologies
thus developed and associated results.
4. Baker B, Banfield J: Microbial communities in acid mine
drainage. FEMS Microbiol Rev 2003, 44:139-152.
A general review describes the microbial communities and diversity
detected in AMD.
Current Opinion in Biotechnology 2016, 38:150–158
156 Environmental biotechnology
5.
Baker-Austin C, Dopson M: Life in acid: pH homeostasis in
acidophiles. Trends Microbiol 2007, 15:165-171.
6.
Johnson DB, Hallberg KB: Carbon, iron and sulfur metabolism
in acidophilic microorganisms. Adv Microb Physiol 2008,
54:201-255.
Kuang JL, Huang LN, Chen LX, Hua ZS, Li SJ, Hu M, Li JT, Shu WS:
Contemporary environmental variation determines microbial
diversity patterns in acid mine drainage. ISME J 2013,
7:1038-1050.
An excellent account of the mechanisms shaping the diversity and
structure of AMD microbial communities, both local scale and global
scale.
7.
8.
Goltsman DSA, Comolli LR, Thomas BC, Banfield JF: Community
transcriptomics reveals unexpected high microbial diversity in
acidophilic biofilm communities. ISME J 2015, 9:1014-1023.
9. Johnson DB, Hallberg KB: The microbiology of acidic mine
waters. Res Microbiol 2003, 154:466-473.
A general review describes the microbial diversity and distribution of
extremophiles in AMD ecosystems.
10. Druschel GK, Baker BJ, Gihring TM, Banfield JF: Acid mine
drainage biogeochemistry at Iron Mountain, California.
Geochem Trans 2004, 5:13-32.
11. Dopson M, Johnson DB: Biodiversity, metabolism and
applications of acidophilic sulfur-metabolizing
microorganisms. Environ Microbiol 2012, 14:2620-2631.
Wales consist of novel and remarkably simple bacterial
communities. Appl Environ Microbiol 2006, 72:2022-2030.
22. Tan GL, Shu WS, Zhou WH, Li XL, Lan CY, Huang LN: Seasonal
and spatial variations in microbial community structure and
diversity in the acid stream draining across an ongoing
surface mining site. FEMS Microbiol Ecol 2008, 70:121-129.
23. Hua ZS, Han YJ, Chen LX, Liu J, Hu M, Li SJ, Huang LN, Shu WS:
Ecological roles of dominant and rare prokaryotes in acid
mine drainage revealed by metagenomics and
metatranscriptomics. ISME J 2014, 9:1280-1294.
A low-abundance AMD community was analyzed using metagenomics
and metatranscriptomics, reconstructing 11 AMD draft genomes using a
powerful ‘divide and conquer’ assembly strategy, and also revealing the
ecological significance of rare taxa.
24. Johnson DB, Hallberg KB, Hedrich S: Uncovering a microbial
enigma: isolation and characterization of the streamergenerating, iron-oxidizing, acidophilic bacterium ‘‘Ferrovum
myxofaciens’’. Appl Environ Microbiol 2014, 80:672-680.
25. Bacelar-Nicolau P, Johnson DB: Leaching of pyrite by
acidophilic heterotrophic iron-oxidizing bacteria in pure and
mixed cultures. Appl Environ Microbiol 1999, 65:585-590.
26. Johnson DB, Rolfe S, Hallberg KB, Iversen E: Isolation and
phylogenetic characterization of acidophilic microorganisms
indigenous to acidic drainage waters at an abandoned
Norwegian copper mine. Environ Microbiol 2001, 3:630-637.
12. Bonnefoy V, Holmes DS: Genomic insights into microbial iron
oxidation and iron uptake strategies in extremely acidic
environments. Environ Microbiol 2012, 14:1597-1611.
27. Liu H, Yin H, Dai Y, Dai Z, Liu Y, Li Q, Jiang H, Liu X: The co-culture
of Acidithiobacillus ferrooxidans and Acidiphilium
acidophilum enhances the growth, iron oxidation, and CO2
fixation. Arch Microbiol 2011, 193:857-866.
13. Rawlings DE, Johnson DB: The microbiology of biomining:
development and optimization of mineral-oxidizing microbial
consortia. Microbiology 2007, 153:315-324.
28. Falagán C, Johnson DB: Acidibacter ferrireducens gen. nov.,
sp. nov.: an acidophilic ferric iron-reducing
gammaproteobacterium. Extremophiles 2014, 18:1067-1073.
14. Méndez-Garcı́a C, Peláez AI, Mesa V, Sánchez J, Golyshina OV,
Ferrer M: Microbial diversity and metabolic networks in acid
mine drainage habitats. Front Microbiol 2015, 6:475.
A review summarizing the microbial diversity and functional networks in
AMD environments, including those from isolation analysis and metaomics data.
29. Ziegler S, Waidner B, Itoh T, Schumann P, Spring S, Gescher J:
Metallibacterium scheffleri gen. nov., sp. nov., an alkalinizing
gammaproteobacterium isolated from an acidic biofilm. Int J
Syst Evol Microbiol 2013, 63:1499-1504.
15. Williams KP, Kelly DP: Proposal for a new class within the
phylum Proteobacteria, Acidithiobacillia classis nov., with the
type order Acidithiobacillales, and emended description of the
class Gammaproteobacteria. Int J Syst Evol Microbiol 2013,
63:2901-2906.
16. Falagán C, Johnson DB: Acidithiobacillus ferriphilus sp. nov.: a
facultatively anaerobic iron- and sulfur-metabolising extreme
acidophile. Int J Syst Evol Microbiol 2015 http://dx.doi.org/
10.1099/ijsem.0.000698.
17. Hedrich S, Johnson DB: Acidithiobacillus ferridurans sp. nov.,
an acidophilic iron-, sulfur- and hydrogen-metabolizing
chemolithotrophic gammaproteobacterium. Int J Syst Evol
Microbiol 2013, 63:4018-4025.
18. Tyson GW, Lo I, Baker BJ, Allen EE, Hugenholtz P, Banfield JF:
Genome-directed isolation of the key nitrogen fixer
Leptospirillum ferrodiazotrophum sp nov. from an acidophilic
microbial community. Appl Environ Microbiol 2005,
71:6319-6324.
19. Goltsman DSA, Denef VJ, Singer SW, VerBerkmoes NC,
Lefsrud M, Mueller RS, Dick GJ, Sun CL, Wheeler KE, Zemla A
et al.: Community genomic and proteomic analyses of
chemoautotrophic iron-oxidizing ‘‘Leptospirillum rubarum’’
(Group II) and ‘‘Leptospirillum ferrodiazotrophum’’ (Group III)
bacteria in acid mine drainage biofilms. Appl Environ Microbiol
2009, 75:4599-4615.
30. Jones RM, Johnson DB: Acidithrix ferrooxidans gen. nov., sp.
nov.; a filamentous and obligately heterotrophic, acidophilic
member of the Actinobacteria that catalyzes dissimilatory
oxido-reduction of iron. Res Microbiol 2015, 166:111-120.
31. Méndez-Garcı́a C, Mesa V, Sprenger RR, Richter M, Diez MS,
Solano J, Bargiela R, Golyshina OV, Manteca A, Ramos JL et al.:
Microbial stratification in low pH oxic and suboxic
macroscopic growths along an acid mine drainage. ISME J
2014, 8:1259-1274.
32. Bond PL, Smriga SP, Banfield JF: Phylogeny of microorganisms
populating a thick, subaerial, predominantly lithotrophic
biofilm at an extreme acid mine drainage site. Appl Environ
Microbiol 2000, 66:3842-3849.
33. Anderson I, Chertkov O, Chen A, Saunders E, Lapidus A, Nolan M,
Lucas S, Hammon N, Deshpande S, Cheng JF et al.: Complete
genome sequence of the moderately thermophilic mineralsulfide-oxidizing firmicute Sulfobacillus acidophilus type
strain (NAL(T)). Stand Genomic Sci 2012, 6:1-13.
34. Travisany D, Di Genova A, Sepulveda A, Bobadilla-Fazzini RA,
Parada P, Maass A: Draft genome sequence of the
Sulfobacillus thermosulfidooxidans Cutipay strain, an
indigenous bacterium isolated from a naturally extreme
mining environment in Northern Chile. J Bacteriol 2012,
194:6327-6328.
35. Justice NB, Li Z, Wang Y, Spaudling SE, Mosier AC, Hettich RL,
Pan C, Banfield JF: 15N- and 2H proteomic stable isotope
probing links nitrogen flow to archaeal heterotrophic activity.
Environ Microbiol 2014, 16:3224-3237.
20. Goltsman DSA, Dasari M, Thomas BC, Shah MB,
VerBerkmoes NC, Hettich RL, Banfield JF: New group in the
Leptospirillum clade: cultivation-independent community
genomics, proteomics, and transcriptomics of the new
species ‘‘Leptospirillum group IV UBA BS’’. Appl Environ
Microbiol 2013, 79:5384-5393.
36. Joe SJ, Suto K, Inoie C, Chida T: Isolation and characterization
of acidophilic heterotrophic iron-oxidizing bacterium from
enrichment culture obtained from acid mine drainage
treatment plant. J Biosci Bioeng 2007, 104:117-123.
21. Hallberg KB, Coupland K, Kimura S, Johnson DB: Macroscopic
streamer growths in acidic, metal-rich mine waters in north
37. Sánchez-Andrea I, Knittel K, Amann R, Amils R, Sanz JL:
Quantification of Tinto River sediment microbial communities:
Current Opinion in Biotechnology 2016, 38:150–158
www.sciencedirect.com
Microbiology ecology in AMD Chen et al. 157
importance of sulfate-reducing bacteria and their role in
attenuating acid mine drainage. Appl Environ Microbiol 2012,
78:4638-4645.
38. Bruneel O, Duran R, Casiot C, Elbaz-Poulichet F, Personne JC:
Diversity of microorganisms in Fe–As-rich acid mine drainage
waters of Carnoules, France. Appl Environ Microbiol 2006,
72:551-556.
39. He Z, Xiao S, Xie X, Zhong H, Hu Y, Li Q, Gao F, Li G, Liu J, Qiu G:
Molecular diversity of microbial community in acid mine
drainages of Yunfu sulfide mine. Extremophiles 2007,
11:305-314.
40. Bertin PN, Heinrich-Salmeron A, Pelletier E, Goulhen-Chollet F,
Arsène-Ploetze F, Gallien S, Lauga B, Casiot C, Calteau A,
Vallenet D et al.: Metabolic diversity among main
microorganisms inside an arsenic-rich ecosystem revealed by
meta- and proteo-genomics. ISME J 2011, 5:1735-1747.
41. Fabisch M, Beulig F, Akob DM, Kusel K: Surprising abundance of
Gallionella-related iron oxidizers in creek sediments at pH
4.4 or at high heavy metal concentrations. Front Microbiol 2013,
4:390.
42. Chen LX, Hu M, Huang LN, Hua ZS, Kuang JL, Li SJ, Shu WS:
Comparative metagenomic and metatranscriptomic analyses
of microbial communities in acid mine drainage. ISME J 2015,
9:1579-1592.
43. Chen LX, Li JT, Chen YT, Huang LN, Hua ZS, Hu M, Shu WS: Shifts
in microbial community composition and function in the
acidification of a lead/zinc mine tailings. Environ Microbiol
2013, 15:2431-2444.
44. Chen YT, Li JT, Chen LX, Hua ZS, Huang LN, Liu J, Xu BB, Liao B,
Shu WS: Biogeochemical processes governing natural pyrite
oxidation and release of acid metalliferous drainage. Environ
Sci Technol 2014, 48:5537-5545.
45. Edwards KJ, Bond PL, Gihring TM, Banfield JF: An archaeal ironoxidizing extreme acidophile important in acid mine drainage.
Science 2000, 287:1796-1799.
46. Tyson G, Chapman J, Hugenholtz P, Allen E, Ram R, Richardson P,
Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF: Community
structure and metabolism through reconstruction of microbial
genomes from the environment. Nature 2004, 428:37-43.
A successful attempt for reconstruction of complete and near-complete
genomes from environmental microbial sample.
47. Golyshina OV, Pivovarova TA, Karavaiko GI, Kondrateva TF,
Moore ER, Abraham WR, Lünsdorf H, Timmis KN, Yakimov MM,
Golyshinet PN: Ferroplasma acidiphilum gen. nov., sp. nov., an
acidophilic, autotrophic, ferrous-iron-oxidizing, cell-walllacking, mesophilic member of the Ferroplasmaceae fam.
nov., comprising a distinct lineage of the Archaea. Int J Syst
Evol Microbiol 2000, 50:997-1006.
48. Dopson M, Baker-Austin C, Hind A, Bowman JP, Bond PL:
Characterization of Ferroplasma isolates and Ferroplasma
acidarmanus sp. nov., extreme acidophiles from acid mine
drainage and industrial bioleaching environments. Appl
Environ Microbiol 2004, 70:2079-2088.
49. Golyshina OV, Timmis KN: Ferroplasma and relatives, recently
discovered cell wall-lacking archaea making a living in
extremely acid, heavy metal-rich environments. Environ
Microbiol 2005, 7:1277-1288.
50. Golyshina OV: Environmental, biogeographic, and biochemical
patterns of archaea of the family Ferroplasmaceae. Appl
Environ Microbiol 2011, 77:5071-5078.
nov., order Thermoplasmatales. Int J Syst Evol Microbiol 2015
http://dx.doi.org/10.1099/ijsem.0.000725.
53. Baker BJ, Tyson GW, Webb RI, Flanagan J, Hugenholtz P,
Allen EE, Banfield JF: Lineages of acidophilic archaea revealed
by community genomic analysis. Science 2006, 314:1933-1935.
54. Baker BJ, Comolli LR, Dick GJ, Hauser LJ, Hyatt D, Dill BD,
Land ML, VerBerkmoes NC, Hettich RL, Banfield JF: Enigmatic,
ultrasmall, uncultivated archaea. Proc Natl Acad Sci U S A 2010,
107:8806-8811.
55. Amaral-Zettler LA, Zettler ER, Theroux SM, Palacios C, Aguilera A,
Amils R: Microbial community structure across the tree of life
in the extreme Rı́o Tinto. ISME J 2011, 5:42-50.
56. Ziegler S, Dolch K, Geiger K, Krause S, Asskamp M, Eusterhues K,
Kriews M, Wilhelms-Dick D, Goettlicher J, Majzlan J et al.:
Oxygen-dependent niche formation of a pyrite-dependent
acidophilic consortium built by archaea and bacteria. ISME J
2013, 7:1725-1737.
57. Aguilera A: Eukaryotic organisms in extreme acidic
environments, the Rı́o Tinto case. Life 2013, 3:363-374.
58. Amaral-Zettler LA: Eukaryotic diversity at pH extremes. Front
Microbiol 2012, 3:441.
59. Das BK, Roy A, Koschorreck M, Mandal SM, Wendt-Potthoff K,
Bhattacharya J: Occurrence and role of algae and fungi in acid
mine drainage environment with special reference to metals
and sulfate immobilization. Water Res 2009, 43:883-894.
60. Parro V, Moreno-Paz M, Gonzalez-Toril E: Analysis of
environmental transcriptomes by DNA microarrays. Environ
Microbiol 2007, 9:453-464.
61. Moreno-Paz M, Gómez MJ, Arcas A, Parro V: Environmental
transcriptome analysis reveals physiological differences
between biofilm and planktonic modes of life of the iron
oxidizing bacteria Leptospirillum spp. in their natural
microbial community. BMC Genomics 2010, 11:404.
62. Schrenk MO, Edwards KJ, Goodman RM, Hamers RJ, Banfield JF:
Distribution of Thiobacillus ferrooxidans and Leptospirillum
ferrooxidans: implications for generation of acid mine
drainage. Science 1998, 279:1519-1522.
63. Schippers A, Sand W: Bacterial leaching of metal sulfides
proceeds by two indirect mechanisms via thiosulfate or
via polysulfides and sulfur. Appl Environ Microbiol 1999,
65:319-321.
64. Küsel K: Microbial cycling of iron and sulfur in acidic coal
mining lake sediments. Water Air Soil Pollut 2003, 3:67-90.
65. Sun W, Xiao T, Sun M, Dong Y, Ning Z, Xiao E, Tang S, Li J:
Diversity of the sediment microbial community in the Aha
Watershed (southwest China) in response to acid mine
drainage pollution gradients. Appl Environ Microbiol 2015,
81:4874-4884.
66. Parro V, Moreno-Paz M: Gene function analysis in
environmental isolates: the nif regulon of the strict iron
oxidizing bacterium Leptospirillum ferrooxidans. Proc Natl
Acad Sci U S A 2003, 100:7883-7888.
67. Ram RJ, VerBerkmoes NC, Thelen MP, Tyson GW, Baker BJ,
Blake IIRC, Shah M, Hettich RL, Banfield JF: Community
proteomics of a natural microbial biofilm. Science 2005,
308:1915-1920.
68. Justice NB, Panb C, Muellera R, Spauldinga SE, Shaha V,
Suna CL, Yeltona AP, Millera CS, Thomasa BC, Shahb M et al.:
Heterotrophic archaea contribute to carbon cycling in low-pH,
suboxic biofilm communities. Appl Environ Microbiol 2012,
78:8321-8330.
51. Golyshina OV, Yakimov MM, Lünsdorf H, Ferrer M, Nimtz M,
Timmis KN, Wray V, Tindall BJ, Golyshin PN: Acidiplasma
aeolicum gen. nov., sp. nov., a euryarchaeon of the family
Ferroplasmaceae isolated from a hydrothermal pool, and
transfer of Ferroplasma cupricumulans to Acidiplasma
cupricumulans comb. nov. Int J Syst Evol Microbiol 2009,
59:2815-2823.
69. Wilmes P, Remis JP, Hwang M, Auer M, Thelen MP, Banfield JF:
Natural acidophilic biofilm communities reflect
distinct organismal and functional organization. ISME J
2009, 3:266-270.
52. Golyshina OV, Lünsdorf H, Kublanov IV, Goldenstein NI,
Hinrichs KU, Golyshin PN: The novel, extremely acidophilic, cell
wall-deficient archaeon Cuniculiplasma divulgatum gen. nov.,
sp. nov. represent a new Family of Cuniculiplasmataceae fam.
70. Gehrke T, Hallmann R, Kinzler K, Sand W: The EPS of
Acidithiobacillus ferrooxidans—a model for structure–
function relationships of attached bacteria and their
physiology. Water Sci Technol 2001, 43:159-167.
www.sciencedirect.com
Current Opinion in Biotechnology 2016, 38:150–158
158 Environmental biotechnology
71. Sand W, Gehrke T: Extracellular polymeric substances mediate
bioleaching/biocorrosion via interfacial processes involving
iron(III) ions and acidophilic bacteria. Res Microbiol 2006, 157:49-56.
75. Johnson DB: Biomining—biotechnologies for extracting and
recovering metals from ores and waste materials. Curr Opin
Biotechnol 2014, 30:24-31.
72. Baker-Austin C, Potrykus J, Wexler M, Bond PL, Dopson M:
Biofilm development in the extremely acidophilic archaeon
‘Ferroplasma acidarmanus’ Fer1. Extremophiles 2010, 14:485-491.
76. Hedrich S, Johnson DB: Remediation and selective recovery of
metals from acidic mine waters using novel modular
bioreactors. Environ Sci Technol 2014, 48:12206-12212.
A description of a well-designed integrated system using AMD microorganisms for AMD remediation and heavy metal recovery.
73. Fang D, Zhou LX: Effect of sludge dissolved organic matter on
oxidation of ferrous iron and sulfur by Acidithiobacillus
ferrooxidans and Acidithiobacillus thiooxidans. Water Air Soil
Pollut 2006, 171:81-94.
74. Silver S, Phung LT: Bacterial heavy metal resistance: new
surprises. Annu Rev Microbiol 1996, 50:753-789.
Current Opinion in Biotechnology 2016, 38:150–158
77. Briones A, Raskin L: Diversity and dynamics of microbial
communities in engineered environments and their
implications for process stability. Curr Opin Biotechnol 2003,
14:270-276.
www.sciencedirect.com