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  • Review Article
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Microbial ecology of expanding oxygen minimum zones

Nature Reviews Microbiology volume 10, pages 381–394 (2012)Cite this article

Subjects

Key Points

  • Oxygen minimum zones (OMZs) are oxygen-starved regions of the ocean that are currently expanding owing to the warming of the water column that is induced by global climate change.

  • Although OMZs are inhospitable to aerobically respiring organisms, these regions support thriving microbial communities, the metabolic activities of which have a profound impact on marine productivity and climate balance.

  • Plurality sequencing combined with process rate measurements and targeted gene surveys in coastal and open-ocean OMZs has identified conserved patterns of microbial community structure and function, and uncovered novel modes of metabolic integration coupling carbon, nitrogen and sulphur cycles. These findings have important implications for our understanding of the ecological and biogeochemical impacts of OMZ expansion.

  • Co-occurrence networks built from taxonomic sequence data can help define putative metabolic interactions among the microorganisms in OMZs and can enable more direct hypothesis testing when combined with data concerning environmental parameters, process rates and functional genes.

  • Determining how these networks form, function and change over time reveals links between microbial community structure and higher-order ecological and biogeochemical processes. This information has the potential to guide human adaptation and response in a time of climate change.

Abstract

Dissolved oxygen concentration is a crucial organizing principle in marine ecosystems. As oxygen levels decline, energy is increasingly diverted away from higher trophic levels into microbial metabolism, leading to loss of fixed nitrogen and to production of greenhouse gases, including nitrous oxide and methane. In this Review, we describe current efforts to explore the fundamental factors that control the ecological and microbial biodiversity in oxygen-starved regions of the ocean, termed oxygen minimum zones. We also discuss how recent advances in microbial ecology have provided information about the potential interactions in distributed co-occurrence and metabolic networks in oxygen minimum zones, and we provide new insights into coupled biogeochemical processes in the ocean.

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Figure 1: O2 concentrations in the ocean.
Figure 2: O2 concentration affects ecosystem energy flow.
Figure 3: Bacterial diversity in the ocean.
Figure 4: Diversity in the four most abundant bacterial groups identified in OMZs.
Figure 5: Co-occurrence networks: correlations among bacterial OTUs in different OMZs.

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Acknowledgements

This work was carried out under the auspices of the Natural Sciences and Engineering Research Council (NSERC) of Canada, the Canada Foundation for Innovation (CFI) and the Canadian Institute for Advanced Research (CIFAR). J.J.W. was supported by the NSERC, and K.M.K. was supported by the Tula Foundation-funded Centre for Microbial Diversity and Evolution (CMDE) at the University of British Columbia, Vancouver, Canada. We thank N. Korniyuk, P. Macoun, V. Tunnicliffe, F. Whitney, M. Robert, A. Hawley and N. Hanson for insightful commentary; D. Walsh for assistance with data visualization; P. Tortell for help with figure 1; and the anonymous reviewers for insightful commentary and guidance.

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Authors and Affiliations

  1. Department of Microbiology and Immunology, University of British Columbia, Life Sciences Institute, 2552–2350 Health Sciences Mall, Vancouver, V6T 1Z3, British Columbia, Canada

    Jody J. Wright, Kishori M. Konwar & Steven J. Hallam

  2. Graduate Program in Bioinformatics, University of British Columbia, Life Sciences Institute, 2552–2350 Health Sciences Mall, Vancouver, V6T 1Z3, British Columbia, Canada

    Steven J. Hallam

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  1. Jody J. Wright
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Correspondence to Steven J. Hallam.

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FURTHER INFORMATION

Steven J. Hallam's homepage

Center for Coastal Margin Observation and Prediction

Genbank

Greengenes taxonomy database

Institute of Ocean Sciences

Leibniz Institute for Baltic Sea Research

Monterey Bay Aquarium Research Institute

The Eastern South Pacific Oxygen Minimum Zone

The Fourth Paradigm: Data-Intensive Scientific Discovery

Victoria Experimental Network Under the Sea (VENUS)

Glossary

Ventilated

Pertaining to the ocean: supplied with atmospheric gases through processes including exchange between the air and sea, exchange between the surface mixed layer and immediate subsurface layer, and circulation in the interior of the ocean.

Thermal stratification

A temperature-layering effect that occurs in water owing to differences in water density: warm water is less dense than cool water and therefore tends to float on top of the cooler, heavier water.

Benthic ecosystems

Ecosystems residing at the lowest level of a body of water such as an ocean or a lake, including the sediment surface and subsurface layers.

Pelagic ecosystems

Ecosystems residing in the region of a body of water that is neither close to the bottom nor near the shore.

Radiative forcing effects

The change in net irradiance between different layers of the atmosphere.

Coastal upwelling

The upwards movement of deep, nutrient-rich water along a coast, caused by wind-driven currents.

Oxycline

A sharp gradient in oxygen concentration that is associated with a redoxcline (a shift in electron donor and acceptor usage).

Eutrophic

Pertaining to a body of water: rich in mineral and organic nutrients.

Eutrophication

Excessive nutrient input to a lake or other body of water (frequently owing to run-off from the land), resulting in explosive plant growth and animal mortality owing to oxygen starvation.

Chemoautotrophic

Capable of using chemical energy to synthesize organic molecules from inorganic substances.

Dissimilatory

Metabolic processes through which elements are oxidized or reduced and for which the organism uses the energy released in the process (catabolism).

Endemism

The ecological state of being unique (endemic) to a defined geographical location, which can be a particular habitat, zone or environment.

Operational taxonomic units

(OTUs). Groups of organisms that are used in phylogenetic studies. An OTU is tentatively assumed to be a valid taxon for purposes of phylogenetic analysis.

Ecotype

A group of organisms within a species that are selectively adapted to a particular set of environmental conditions and therefore exhibit behavioural, structural or physiological differences from other members of the species.

Heterotrophic

Dependent on obtaining carbon for growth and energy from complex organic compounds.

Entner–Doudoroff pathway

An alternative series of reactions for the catabolism of glucose to pyruvate, using a different set of enzymes from those used in either glycolysis or the pentose phosphate pathway.

Dark ocean

The depths of the ocean beyond which less than 1% of sunlight penetrates; also known as the aphotic zone.

Syntrophy

Metabolite exchange that occurs between two or more groups of organisms and is necessary for cell growth or energy production.

Chemolithoautotrophic

Capable of obtaining energy from the oxidation of inorganic compounds and carbon from the fixation of carbon dioxide.

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Wright, J., Konwar, K. & Hallam, S. Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol 10, 381–394 (2012). https://doi.org/10.1038/nrmicro2778

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