Available online at www.sciencedirect.

com

Microorganisms and their roles in fundamental

biogeochemical cycles
Eugene L Madsen

Biogeochemistry is the discipline that strives to understand The term ‘‘biotechnology’’ originated in 1917 when used
intricate processes, often microbially mediated ones, that by a Hungarian engineer, Karl Ereky, in reference to the
transform and recycle both organic and inorganic substances integration of biological processes to achieve a desired
in soils, sediments, and waters. These processes, goal [4]. ‘‘Environmental biotechnology’’ has recently
manifestations of diverse and highly evolved cellular been defined as ‘‘the integrated use of biochemistry,
mechanisms catalyzed by Bacteria and Archaea, maintain the molecular biology, genetics, microbiology, plant and
biosphere. Progress in biogeochemistry relies upon the animal science, and chemical engineering to addresses
underlying science of environmental microbiology. Over the environmental needs and problems’’ [5].
last 2 years, important discoveries have advanced the
ecological, physiological, biochemical, and genomic bases for The central thesis of this essay is that ‘‘biogeochemistry’’
a variety of microbiological processes including anaerobic and ‘‘environmental biotechnology’’ are converging dis-
methane oxidation, photosynthesis, phosphorous uptake, ciplines. This is because the mechanistic understanding
biodegradation of organic pollutants, and numerous aspects of of relatively simple biological systems that has fostered
the nitrogen and sulfur cycles. Here recent literature is the creation of biotechnology is being extended to com-
assessed and placed within a five-stage paradigm for making plex naturally occurring microbial communities that dwell
scientific progress in environmental microbiology, in the waters, sediments, and soils. It is these microbial
biogeochemistry, and biotechnology. communities that maintain the biosphere through the
biogeochemical reactions they catalyze. Modern biogeo-
Address chemistry, like biotechnology, demands fundamental
Cornell University, Department of Microbiology, B57A Wing Hall, Wing mechanistic knowledge of the genomic, genetic, enzy-
Drive, Ithaca, NY 14853, United States matic, biochemical, and physiological bases of a plethora
Corresponding author: Madsen, Eugene L (elm3@cornell.edu)
of microbially mediated processes (e.g. ranging from
photosynthesis to sulfate reduction to nitrogen fixation).
Such knowledge provides a deep level of understanding,
Current Opinion in Biotechnology 2011, 22:456–464 which is the gateway to two important goals: (i) wise and
efficient management of ecosystems, and (ii) potential
This review comes from a themed issue on
Environmental biotechnology exploitation of the process for attaining new or improved
Edited by Lindsay Eltis and Ariel Kushmaro services or technologies.

Available online 16th February 2011 The objective of this review is to begin to substantiate the
0958-1669/$ – see front matter above-suggested convergence between biotechnology and
# 2011 Elsevier Ltd. All rights reserved. biogeochemistry by proposing a five-stage paradigm for
inquiry and then reviewing key recent advances in the
DOI 10.1016/j.copbio.2011.01.008
discipline that underlies biogeochemistry: environmental
microbiology. The scope of biogeochemistry and environ-
mental microbiology is so broad as to prevent a compre-
hensive review of these topics. However, key publications
Introduction: biogeochemistry is advanced by
from 2009 to 2010, illustrative of how environmental
environmental microbiology and is converging
microbiology discoveries are made, will be highlighted.
with environmental biotechnology
The term ‘‘biogeochemistry’’ was first coined by V.
Vernadsky in 1926 (cited in [1]). Explicit in ‘‘biogeo- Biogeochemical processes and how they
chemistry’’ is the merging (the linking) of three scientific maintain the biosphere
disciplines: biology, geology, and chemistry. Other pro- From a scale of cubic centimeters to one of the entire
minent authors [2,3] have extended and reinforced the planet, Earth habitats can be viewed as complex mixtures
immanent traits, the realities, of how ecosystems function of reduced and oxidized materials in chemical disequili-
at local and global scales. Multidisciplinary biogeochem- brium [5,6]. Ultimately, this disequilibrium is maintained
ical approaches are the way to understand complex pro- by constant influx of radiant energy from the sun, and
cesses that occur in forested watersheds, coastal constant efflux of heat and reduced materials (e.g. CH4,
sediments, agriculture fields, grasslands, oceans, other H2S, H2) from the Earth’s core [5]. This disequilibrium
habitats, and the entire biosphere, itself. has driven life processes and evolution for nearly 4 billion

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 Microorganisms and their roles in fundamental biogeochemical cycles Madsen 457

years [5,6]. Energetically favorable chemical reactions occurs) are passed through a series of molecular carriers
yield free energy that can be translated into proton motive in a membrane-bound electron transport chain, ultimately
force which, in turn, drives the synthesis of ATP, the on to O2, which is reduced to H2O. Figure 1 provides a
universal energy currency for cellular processes. Such general paradigm for the diversity of oxidation-reduction
reactions provide very strong selective pressures that have reactions mediated by microorganisms that dwell in soils,
led to the evolution of sophisticated biochemical pro- sediments, and waters that comprise the biosphere. Over
cesses such as cellular respiration. The sets of energeti- evolutionary time, an astounding array of metabolic path-
cally favorable reactions that occur throughout the ways mediating the thermodynamically favorable permu-
biosphere are site-specific (at the scale of micrometers) tations of electron-donor/electron acceptor pairs has
and they are dynamic in time. The reduced materials are, developed. By exploiting such reactions for ATP pro-
by definition, electron donors that react in thermodyna- duction, microorganisms (especially Bacteria and Archaea)
mically predictable patterns often termed ‘‘oxidation- that dwell in biosphere habitats recycle nutrients and
reduction’’ or ‘‘redox’’ processes which link two ‘‘half biomass. These, along with ATP-consuming biosynthetic
reactions’’ together [5,6]. reactions such as fixation of C (photosynthesis) and N
(nitrogen fixation), are the biogeochemical reactions that
A very familiar pair of half reactions is known as ‘‘carbon cause the cycling of carbon-rich, nitrogen-rich, sulfur-rich
respiration’’ (Box 1, top). In this process a reduced form of and other materials (Figure 1). When integrated, in time
carbon such as glucose is the electron donor: it yields and space, these individual steps lead to the complete
electrons as the carbon atoms are oxidized to CO2. If cycling (from highly reduced forms to highly oxidized and
oxygen is present in a given habitat, it is likely that native back) of many elements. This linkage between steps
organisms will use the oxygen gas as an electron acceptor constitutes the ‘‘biogeochemical cycles’’. A selection of
to drive respiratory ATP production. The electrons widely recognized processes contributing to the biogeo-
yielded by C atoms in glucose (as oxidation to CO2 chemical cycles (e.g. for N, nitrification, denitrification,

Box 1 Background definitions, terms, and key tools used in biogeochemistry and environmental microbiology

 A sampling of broadly recognized biogeochemical processes

Nutrient cycle Process Operational definition
Carbon Photosynthesis Light-driven CO2 fixation into biomass
Carbon Respiration Oxidation of organic C to CO2
Methanogenesis Methane production
Aerobic methane oxidation Methane becomes CO2
Anaerobic methane oxidation Methane becomes CO2
Nitrogen Nitrogen fixation N2 gas becomes ammonia
Ammonium oxidation Ammonia becomes nitrite, nitrate
Anaerobic ammonium oxidation Nitrite and ammonia become N2 gas
Denitrification Nitrate is used as an electron acceptor and converted to N2 gas
Sulfur Sulfur oxidation Sulfide and sulfur become sulfate
Sulfate reduction Sulfate is used as an electron acceptor and converted to sulfur and sulfide
Other elements Hydrogen oxidation Hydrogen is oxidized to H+, electrons reduce other substances
Uranium reduction Uranium oxycation is used as an electron acceptor; hence immobilized
Iron reduction Ferric ion is used as electron acceptor and converted to Fe2+

 Five key approaches in environmental microbiology ‘‘tool box’’

Site geochemistry: Analytical chemistry proves presence of compounds indicative of microbial process (reinforced by flux data and
isotopic fractionation patterns).
Cultivation: Provision of appropriate nutrients in liquid or solid media allows isolation of microorganisms catalyzing process
of interest (e.g. denitrification or benzene biodegradation).
Incubations: Placing environmental samples or pure cultures in sealed, laboratory vessels allows documentation of physiological
changes (e.g. methane generation or consumption) effected by microorganisms.
Biomarkers: Extraction and analysis of key cellular constituents. These provide insights into the taxonomic composition and/or
functional potential of microorganisms by focusing upon phospholipid fatty acids, DNA, ribosomal RNA, messenger
RNA, or proteins followed by GC/MS, LC/MS and/or various molecular biology procedures ranging from small-scale
sequencing to high-throughput meta-genomics, meta-transcriptomics, and meta-proteomics.
Microscopy: Allows images of microorganisms and cell associations to be obtained from site samples or laboratory incubations.
Depending upon analytical approach and staining targets, information yielded includes enumeration, identity
(e.g. via small subunit rRNA FISH probes), localization of biomarkers within cells, and cell-specific substrate
incorporation (e.g. via secondary ion mass spectrometry).

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458 Environmental biotechnology

Figure 1

Thermodynamics [Defines energetically favorable reactions]

Geochemistry [Governs site-specific redox conditions and physiology]

Electron donors Microbially mediated electron Electron acceptors
(reduced) transport (oxidized)

Element Compound Element Compound

C CH4 C CO2
C8H18 CH2O
CH2O C2Cl4

N NH3 N NO3-
N 2O e- NO2-

S H 2S S SO42-
So S2O32-

Other H2 Other O2
Fe2+ Fe3+
Mn2+ Mn4+
ATP
and
Cell Growth

Current Opinion in Biotechnology

Conceptual view of how microorganisms catalyze biogeochemical reactions between electron donors and electron acceptors that occur in habitats
such as soil, sediments, and waters. The specific reactions that occur in a given habitat are governed by both local geochemistry and the laws of
thermodynamics. Each electron donor ‘‘half reaction’’ (upper curved arrow, center) must be coupled to an electron acceptor ‘‘half reaction’’ (lower
curved arrow, center).

and anammox) are defined in Box 1. It is important to note substrates (e.g. oxygen, ferric iron, nitrate) and local
that the cycles of C, N, S and other elements (Figure 1, microbial populations ‘‘make a living’’ by completing
Box 1) are intimately linked. For example, as reduced electron donor-electron acceptor reactions, thereby, gen-
forms of carbon are oxidized in an oxygen-free habitat, erating energy and growing new cells (Figure 1). The
electron flow may eventually be used by indigenous reduced byproducts of such reactions (e.g. organic acids,
microbial communities (often with H2 gas as an inter- Fe2+, ammonia) can then diffuse to a new geochemical
mediate) to reduce nitrate to N2 (denitrification) or sul- context containing electron acceptors and the byproducts,
fate to sulfide (sulfate reduction) or carbon dioxide to themselves, can then be used as electron donors by other
methane (methanogenesis) or Mn4+ to Mn2+ (manganese microbial populations. The above-described sequences of
reduction). processes maintain order and homeostasis in the bio-
sphere [5,6]. But, two facts need to be recognized: (i)
How advancements are made: five stages in the system of interacting biogeochemical reactions is
understanding complex processes in natural highly complex, poorly characterized, and mediated by
systems a vast unknown diversity of microorganisms, and (ii) the
The complex local and global biogeochemical reactions cycles are increasingly susceptible to disruption by
that are catalyzed by microorganisms occur spon- human activity; thus, understanding mechanistic details
taneously, day-by-day, minute-by-minute, in soils, sedi- is ever pressing to assist in ecosystem management de-
ments, and waters. When a tree falls in the forest, or cisions.
sulfide is released from an oceanic hydrothermal vent,
microorganisms are there. The reduced substrates (e.g. Environmental microbiology is a discipline that encom-
plant biomass and H2S) are comingled with oxidized passes many goals; among them is discovering mechan-

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 Microorganisms and their roles in fundamental biogeochemical cycles Madsen 459

istic bases of the biogeochemical reactions that occur methods and strategies proliferate in the post-genomic
in soils, sediments, and waters. Five major types of era, alternative but equivalent means of attaining Stage 2
analytical, microbiological, and/or molecular tools are are developing. Once a model system has been imple-
routinely used to advance environmental microbiology: mented in laboratory culture, then tools including micro-
site geochemistry, cultivation, incubations, biomarkers, scopy, biomarker sequencing (linked to bioinformatic
and microscopy (see Box 1, bottom). These tools are analysis), isotopic tracers, analytical chemistry, and enzy-
applied in varied proportions throughout what are mology, can be used to decipher both microbial associ-
formally proposed here to be the five stages of environ- ations essential for the process and the biochemical
mental microbiological inquiry leading to advances in mechanisms of the process (Stage 3). Among the key
biogeochemistry: types of information yielded by Stage 3 investigations are
proteins, DNA signatures, mRNA signatures, character-
 Stage 1. Discovery of new microbiological process. Prove istic metabolites, and other biomarkers that can be used in
that microorganisms are capable of catalyzing the verifying the ecological relevance and geographical
process of interest. This is achieved via laboratory prevalence of the process in the original field study site
incubation of environmental samples and/or via and perhaps in globally distributed analogs of that field
chemical or biomarker assays performed on complex, study site (Stage 4). A recently successful example of
uncharacterized microbial communities accompanied Stage 5 (biotechnological application) is the use of
by materials from soils, sediments, or waters. anaerobic ammonium oxidation (anammox) to treat
 Stage 2. Validation of the discovery by finding representative high-ammonia-containing wastewater effluent [7].
microbiological agents. Refine the test system by isolating
a single microorganism capable of catalyzing the A selection of prominent recent environmental
process or obtaining a simplified, highly enriched microbiology studies
consortium of microbial populations exhibiting the Contributions to the field of environmental microbiology
process or via a convincing combination of biomarkers addressing biogeochemistry constantly appear in disci-
and physiological evidence. pline-specific journals (e.g. Applied and Environmental
 Stage 3. Characterization of agents and the physiological, Microbiology, Environmental Microbiology, ISME Journal,
biochemical, and/or genomic mechanisms of the biogeochem- Geomicrobiology, Geobiology, FEMS Microbiology Ecology,
ical process(es) they catalyze. Use of controlled laboratory Microbial Ecology) and in broader, higher-profile journals
incubations, chemical assays, isotopic tracers, bio- (Proceedings of the National Academy of Sciences, Science, and
markers (see Box 1), and often bioinformatics to define Nature). Using the five-stage scheme above, I have classi-
metabolites, metabolic pathways, enzymatic reactions, fied and grouped studies representative of trends and new
and the genetic basis of cellular processes. developments with broad impact on both biogeochem-
 Stage 4. Field verification of ecological relevance of agents istry and environmental microbiology (Table 1).
and/or their biogeochemical impact. Apply the tools,
insights, biomarker analyses from Stage 3 to real-world Four entries appear in the initial discovery category
field sites where microbiological agents (specific taxa (Stage 1) of Table 1. Of these, only Beal et al. [8] (entry
and/or their functional genes) are influencing ecological #1) conforms perfectly to the classic approach of bringing
conditions. an environmental sample into the laboratory and applying
 Stage 5. Biotechnological innovation and/or improved site analytical chemistry procedures to document a previously
management based on understanding biogeochemical process undescribed physiological process mediated by microor-
mechanisms. In some instances microbial-mediated ganisms. For decades it has been acknowledged that it is
processes can be transplanted from their ecosystem thermodynamically feasible for microorganisms to use
contexts to human-engineered settings for commercial methane as an electron donor and both Mn-oxide and
or industrial applications. Fe-oxide as electron acceptors. Beal et al. [8] were the
first to select the right environmental samples, featuring
The path from initial discovery of microbially mediated the right native microbial community, incubated under
biogeochemical processes (Stage 1) through to their bio- the right conditions, analyzed with the right procedures.
technological applications (Stage 5) begins in field study Stages 2–5 are sure to gradually unfold in the future for
sites where biogeochemical processes are suspected to Mn-based and Fe-based oxidation of methane. Entries
occur in their native ecological settings. These ecological #2–4 in Table 1 (respectively addressing: linkage be-
settings pose many challenges for deciphering and doc- tween dissimilatory reduction of nitrate to ammonia
umenting geochemical change within complex environ- and the oxidation of both aromatic hydrocarbons and
mental matrixes containing thousands of microbial ammonia, polychlorinated biphenyl (PCB) biodegrada-
species. Arguably, the most important of these challenges tion, and regulatory small RNAs in biogeochemically
is the difficulty of isolating a single microbial culture (or a active ocean microbial communities) relied on the
defined mixture of cultures) that replicate the biogeo- analysis of either environmental transcripts (mRNA
chemical process in the laboratory (Stage 2); as new expressed in a field site), or structural genes (DNA), or

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460 Environmental biotechnology

Table 1

Survey of recent environmental microbiological studies advancing knowledge of biogeochemistry. The stages of discovery correspond to
those described in the text

Stage of inquiry Entry Biogeochemical Habitat Key findings Reference

process(es)
1. Discovery 1 Mn-dependent and Fe- Ocean sediment Production of 13CO2, from 13C-methane was [8]
dependent oxidation of enhanced by addition of Mn-oxide and Fe-oxide
methane (anaerobic) in 4-month laboratory incubations; comparison
of clone libraries [16S rRNA and
methanogenesis (mcrA) genes] gave clues about
active populations
2 Linkage between carbon Contaminated The pool of mRNA in an aquifer contaminated [9]
and nitrogen cycles: groundwater with aromatic hydrocarbons showed in situ
aromatic hydrocarbon expression of aromatic biodegradation and N-
oxidation, dissimilatory cycle-related genes; ammonia was also
reduction of nitrate to enriched in the groundwater
ammonia (DNRA) and
nitrification
3 Aromatic hydrocarbon Polychlorinated New genetic diversity as revealed by high [10]
oxidation biphenyl- throughput (454 Pyro) sequencing of PCR-
contaminated soil amplified biphenyl dioxygenase genes; >2600
adjacent to tree sequences yielded 25 novel clusters of
roots dioxygenase genes
4 Potential regulation of Ocean waters High throughput (454 Pyro) sequence of the [11]
carbon, nitrogen, and mRNA pool gathered from four ocean depths
phosphorous cycling showed sequence of previously unknown small
RNAs likely to be important regulatory elements
within microbial populations controlling oceanic
C-, N-, or P-cycles
2. Validation 5 P uptake and assimilation Ocean water P uptake and assimilation into phytoplankton [12]
lipids was measured in samples of both
Sargasso Sea (<10 nmol/L P) and the South
Pacific (>100 nmol/L P); the phytoplankton
synthesize non-phosphorous ‘‘substitute lipids’’
when adapting to P scarcity
6 Oxidation of sulfur, Anaerobic ocean The metagenome of a ubiquitous microbe [13]
reduction of nitrate, CO2 water (SUP05) was assembled — providing a
fixation metabolic map of its likely biogeochemical roles
in oxygen-depleted marine waters
7 Photosynthesis, N2 Trichodesmium (a High throughput (454 pyro) sequencing of the [14]
fixation, S metabolism, P cyanobacterium) mRNA pool yielded 5711-day and 5385-night
uptake, arsenic in Ocean water mRNA sequences; P-limitation stress was
detoxification indicated in Trichodesmium; the majority of
transcripts were from co-occurring microbes:
cyanobacteria, heterotrophic bacteria,
eukaryotes, and phage
8 Nitrogen fixation, transfer Ocean sediment Microscopic imaging (fluorescent in situ [15]
of fixed N to associated hybridization and nanometer secondary-ion
microbes in consortium mass spectrometry) of incorporated 15N from
15
that oxidizes methane N2 into cell biomass and N transfer from one
using sulfate as electron cell type to another
acceptor
9 Photosynthesis and N2 Ocean water Whole genome sequencing of DNA was [16]
fixation in a widely completed for 5000 cells from sea water; data
distributed uncultivated showed absence of oxygen-producing photo-
marine microbe, UCYN-A system II, a nitrogen fixation pathway, and a
small (1.44 Mb) genome lacking many
biosynthetic pathways (implying metabolic
dependence upon other organisms)
Mechanism 10 Aerobic oxidation of Ocean water Genome sequence of Nitrosopumilus maritimus [17]
ammonia to nitrate revealed highly copper-dependent systems for
(nitrification) by a recently ammonia oxidation and electron transport that
isolated ubiquitous are distinct from known ammonia oxidizing
member of the marine Bacteria
Archaea

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 Microorganisms and their roles in fundamental biogeochemical cycles Madsen 461

Table 1 (Continued )
Stage of inquiry Entry Biogeochemical Habitat Key findings Reference
process(es)
11 Nitrification by Ocean water Kinetic and biochemical characterization of N. [18]
Nitrosopumilus maritimus maritimus shows remarkably high specific
affinity for ammonium, explaining its likely
ecological role as nitrifier in the oligotrophic
ocean
12 Oxygen production and Freshwater soil Genomic, transcriptomic and proteomic [19]
nitrite-driven anaerobic and sediment procedures were used to discover the
methane oxidation mechanism by which an enrichment culture
carries out nitrite-dependent anaerobic methane
oxidation; nitrite reduction pathways were
absent; instead, oxygen-dependent methane-
oxidation pathways were present; nitrite-
dependent oxygen production was documented
and a pathway converting NO to O2 and N2 was
proposed.
13 P uptake as selective Ocean water Completed genomes of two ubiquitous marine [20]
pressure in oligotrophic photosynthetic bacteria (Prochlorococcus and
seawater Pelagibacter) were used to interpret
metagenomic surveys of the Sargasso Sea (P-
limited) and the North Pacific; cross-habitat
comparison showed P availability to be in the
dominant selective pressure causing divergence
of pan-oceanic populations
Field verification 14 Entire N cycle [ammonia Ocean water near Geochemical and physiological and quantitative [21]
oxidation, nitrate- Peru determination of both structural genes and their
reduction, anammox, transcripts at three depths in four locations off
dissimilatory nitrite the Peruvian Coast; findings document a new
reduction to ammonia variant of the N cycle in which DNRA supplies
(DNRA)] ammonium to the anammox portion of the cycle
15 Denitrification versus Arabian Sea Measurements included geochemical depth [22]
anammox profiles, physiological rates of anammox versus
denitrification, and quantification of genes
indicative of anammox and denitrification; in
seven of eight experiments denitrification was
responsible for 87–99% of total N2 production
16 Aerobic ammonia Ocean water Long-term monitoring (2003–2006) of three [23]
oxidation (Nitrification) (Southern depths was completed for geochemical and
Californian Bight) microbial-community profiles and for copies of
genes indicative of Archaea and ammonia
oxidation genes; trends show population
dynamics and decoupling of ammonia and nitrite
oxidation
17 Biodegradation of Contaminated Sixteen-year record shows diminishing [24]
aromatic hydrocarbons groundwater concentrations of aromatic contaminants;
community 16S rRNA fingerprints show dynamic
system; small subunit rRNA sequences
indicated an extensive microbial food chain,
including eukaryotes
18 Flow of electric current Anaerobic marine Geochemical profiles in Danish harbor [25]
sediments sediments and time-series responses of O2 and
H2S during oxic-anoxic cycles were measured;
the rapid system responses could not be
explained by chemical diffusion; instead
extracellular conductivity (perhaps via microbial
nanowires) were evoked
19 Sulfide oxidation linked to Anaerobic marine A 7,000 km2 area of the African shelf was [26]
nitrate reduction waters off coastal detoxified of its sulfidic waters by a bloom of
western Africa sulfide oxidizing bacteria; data gathered
included geochemical profiles, stoichiometric
modeling, physiological incubations,
sequencing of 16S rRNA and sulfide oxidizing
genes, and microscopic enumeration of sulfide-
oxidizing bacteria

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462 Environmental biotechnology

Table 1 (Continued )
Stage of inquiry Entry Biogeochemical Habitat Key findings Reference
process(es)
20 Iron and sulfate Oceanic The International Ocean Drilling Program [27]
reduction, acetate subsurface produced vertical geochemical profiles and
oxidation, sediments sediment samples analyzed by microscopy, 16S
methanogenesis rRNA community gene profiles, physiological
incubations, and quantitative PCR of genes
indicative of Archaea, Bacteria, Geobacter,
dissimilatory sulfite reductase and
methanogenesis
Biotechnology 21 Generation of electric Various habitats, Promising technologies rely upon innate [28]
innovation current including adaptations (nanowires, extracellular electron
sediments and carriers, etc.) by anaerobic bacteria for
bioreactors transferring electrons to surfaces of insoluble
electron acceptors; engineered microbial fuel
cells are under development
22 Anaerobic ammonium Various The ability of microorganisms to use ammonium [29]
oxidation (Anammox) freshwater and as electron donor and nitrite as electron
other sediments acceptor to produce N2 has led to commercial
and bioreactors reactors that economically treat high-strength
industrial ammonium waste waters

both to gain insight into the metabolic functioning of cycling of N, O, C, and P (entries #10–13, Table 1).
naturally occurring microbial communities. Long-standing questions about the biogeochemical role
of broadly disseminated Archaea in the world’s oceans
Regarding the second stage of biogeochemical inquiry in were addressed by entries #10 and #11: analysis of the
Table 1, entries #5–9 validate, confirm, or extend infor- genome of Nitrosopumilus maritimus revealed a novel
mation about previously reported processes. Pertinent to aerobic ammonium oxidation mechanism, while kinetic
the P cycle, entry #5 used biochemical characterization and biochemical measurements on N. maritimus proved
procedures to show the photosynthetic (phytoplankton) its ability to successfully take up and oxidize ammonia
portion of oceanic microbial communities is capable of at the low concentrations that prevail in ocean waters.
adapting to extreme P scarcity by substituting non-P- Entry #12 provides a remarkable example of how bioin-
containing lipids in cellular membranes. Entry #6 used formatic interpretation of nucleic acid and proteome
bioinformatic analysis of environmental DNA (metage- data from a mixed-enrichment culture (that anaerobi-
nomics) to assemble evidence about the probable phys- cally oxidizes methane using nitrite/nitrate as the elec-
iological role of an uncultivated marine microorganism tron acceptor) can lead to the discovery of a previously
previously show to flourish in oxygen-depleted zones of unrecognized enzymatic process: the conversion of NO
the ocean. Entry #7 analyzed environmental mRNA to N2 and O2. Entry #13 of Table 1 reports the use of
(metatranscriptomics) extracted from the raft-forming comparative genomics and DNA sequence analysis
cyanobacterium, Trichodesmium, harvested from Pacific from microbial communities in low-P and high-P areas
surface waters: insights into the in situ physiological status of the world oceans: Coleman and Chisholm [20]
and nutrient stresses of the associated community (from showed that P availability is the predominant driving
viruses to eukaryotes) were revealed. High-resolution force for genomic divergence of Prochlorococcus and
mass spectrometric (nanoSIMS) imaging of the compo- Pelagibacter populations dwelling in the Sargasso Sea
sition of individual bacterial cells (entry #8) allowed and North Pacific.
Dekas et al. [15] to prove that one member of a con-
sortium of microbial types known to anaerobically oxidize The field verification section (Stage 4) in Table 1 features
methane also fixed 15N2 into its cell biomass and then three studies addressing the N cycle. Entry #14 presents
shared that fixed nitrogen with another member of the comprehensive, nearly revolutionary assembly of geo-
consortium. Finally, analysis of a completed 1.44 Mb chemical, physiological, and nucleic acid (both DNA
genomic sequence of a widespread uncultured photosyn- and mRNA) assays establishing dissimilatory nitrate
thetic marine cyanobacterium revealed its likely physio- reduction to ammonia (DNRA) and anammox as essential
logical niche, which includes the absence of O2 links in nitrogen cycle off the Peruvian Coast. Ward et al.
generation and nutritional dependence upon neighboring [22] (entry #15) showed the predominant pathways of
cells in its community (entry #9, Table 1). electron flow in the oxygen-depleted zone of the Arabian
Sea is denitrification (not anammox). Beman et al. [23]
Research advancing the mechanistic details of micro- (entry #16) used long-term monitoring of geochemistry
bially mediated biogeochemical reactions addressed the and the composition and abundance of ammonia oxi-

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 Microorganisms and their roles in fundamental biogeochemical cycles Madsen 463

dation genes to establish a link between Archaea and management and the development of new biotechnol-
nitrification. Yagi et al. [24] (entry #17) provided a 16- ogies.
year record of contaminant-loss data and linked this
biodegradation process to dynamic microbial commu-
nities that included an extensive food chain involving Acknowledgement
protozoan predation. Entry #18 [25] raises the possibility During preparation of this manuscript, the author’s research was supported
by the National Science Foundation grant #DEB-0841999.
that recent reports of extracellular electron transfer by
anaerobic bacteria may have broad-scale ecological sig- References and recommended reading
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extensive teams together to examine site-specific have been highlighted as:
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based oxidation of a potentially toxic plume of hydrogen  of outstanding interest
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464 Environmental biotechnology

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