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Microbial ecology of Antarctic aquatic systems

An Erratum to this article was published on 20 October 2015

This article has been updated

Key Points

  • The application of 'omic' approaches (for example, pyrosequencing, metagenomics, metatranscriptomics and metaproteomics) has generated unprecedented insight into Antarctic microorganisms and revealed intriguing properties about communities that can be linked to their Antarctic-specific habitats.

  • Community composition and ecosystem function are controlled by the polar light regime, biotic and abiotic environmental factors, limnological history and seed populations, biogeography and the limits of aeolian and advective dispersal caused by physical barriers and distance between sites, and perturbation caused by ecosystem change.

  • The polar austral summer is characterized by continuous high solar irradiance, which stimulates phototrophic growth and kinetically accelerates growth. Such communities tend to be oriented towards maximizing the effectiveness of light energy while switching to light-independent processes (for example, chemolithoautotrophy, phagotrophy and heterotrophic utilization of storage compounds) to survive the cold, dark winter.

  • Virus–host interactions are particularly important in the Antarctic food web, in which they not only control remineralization and influence community composition but have unanticipated roles in influencing productivity cycles. Discoveries pertaining to viruses have included systems with a high diversity of novel eukaryotic viruses, phage-resistant bacteria, and archaea capable of evading, defending against and adapting to viruses.

  • Unusual biogeochemical cycles have developed as a result of communities evolving in very specific, local environments. The indigenous communities have developed a range of traits, including a hierarchical structure, low complexity, niche adaptation, clonal dominance, mixotrophy and short-circuited nutrient cycles that enhance the use and conservation of resources.

  • Specific taxa have a major influence on overall ecosystem function, with stability of those biomes being reliant on the key, specialized and fit members maintaining function and not being affected by ecosystem perturbation, particularly anthropocentric climate change and the introduction of alien species.

Abstract

The Earth's biosphere is dominated by cold environments, and the cold biosphere is dominated by microorganisms. Microorganisms in cold Southern Ocean waters are recognized for having crucial roles in global biogeochemical cycles, including carbon sequestration, whereas microorganisms in other Antarctic aquatic biomes are not as well understood. In this Review, I consider what has been learned about Antarctic aquatic microbial ecology from 'omic' studies. I assess the factors that shape the biogeography of Antarctic microorganisms, reflect on some of the unusual biogeochemical cycles that they are associated with and discuss the important roles that viruses have in controlling ecosystem function.

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Figure 1: Overview of Antarctica.
Figure 2: Vestfold Hills lakes.
Figure 3: McMurdo Dry Valleys lakes.
Figure 4: Unusual Antarctic biogeochemistry.
Figure 5: Overview of Antarctic lake ecology.

Change history

  • 20 October 2015

    In the above article, there were two spelling errors. The credit line for Figure 2e should read: "Image of Deep Lake courtesy of M. Milnes, Australian Antarctic Division." The acknowledgments should read: “The author is indebted to ... M. Milnes ... for providing images of Antarctic lakes...” These have now been corrected in the online version of the article. We apologize to the readers for any misunderstanding caused.

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Acknowledgements

The author is indebted to J. Berengut and D. Smith who crafted figures, A. Hull, M. Milnes, H. Dugan and J. Mikucki for providing images of Antarctic lakes, the Landsat Image Mosaic of Antarctica (LIMA) project for making satellite images available, D. Velázquez for discussions about Antarctic viruses, and T. Kolesnikow and T. J. Williams for insightful comments on manuscript drafts. The author's Antarctic research has been supported by the Australian Research Council, the Australian Antarctic Science Program, the Gordon and Betty Moore Foundation for DNA sequencing at the J. Craig Venter Institute and the US Department of Energy for DNA sequencing at the Joint Genome Institute.

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PowerPoint slides

Glossary

Antarctic thermohaline circulation

Antarctic thermohaline circulation (part of 'the global conveyer belt') arises from katabatic winds — which cause water movement that cools Southern Ocean water, which sinks because of its increased density — and from sea ice formation, which results in salt exclusion, causing the sinking of dense briny water.

Antarctic ice sheet

The Antarctic continent comprises the Antarctic Peninsula Ice Sheet, the West Antarctic Ice Sheet and the East Antarctic Ice Sheet, which collectively comprise more than 500 individual glaciers.

Stratification

The difference in the density of water between the surface and deeper waters (for example, upper ocean stratification from the surface to a depth of 200 m); stratification is increasing owing to the warming of surface waters and to an increase in freshwater content in high-latitude regions.

Endemicity

The extent to which isolation and natural selection affect speciation of microorganisms in a given region (in this case, within Antarctica).

Pelagic

Pelagic microorganisms inhabit the open ocean, in contrast to sea-ice microorganisms, which inhabit sea ice.

Krill

Crustaceans (euphausiids) that live in the open ocean, feed on phytoplankton and to some extent zooplankton, and represent an important component in the food web bridging microorganisms (for example, primary producers) and higher trophic organisms (for example, fish, whales, seals and seabirds) that depend on them for survival.

Pyrosequencing

Targeted DNA sequencing of specific gene amplicons, typically regions of small subunit rRNA (SSU rRNA) genes that can subsequently be used for generating diversity estimates and phylogenetic reconstruction of microbial community composition.

Metagenomics

The study of the total DNA sequences obtained from DNA extracted from an environmental sample, with random 'shotgun' sequencing providing an inventory of genes representing the organisms present within the sample.

Metatranscriptomics

The study of RNA species expressed by a microbial community present within an environmental sample determined by DNA sequencing of reverse transcribed cDNA generated from the RNA.

Metaproteomics

The study of the proteins represented by a community of microorganisms present in an environmental sample, with protein identifications obtained using mass spectrometry to determine the mass of peptides derived from extracted proteins.

Microbial communities

All individual microbial taxa within a defined habitat.

Advection

Physical transport of components (for example, biotic and abiotic matter and heat) by ocean currents.

Biogeography

Distribution of biodiversity over space and time.

SAR11 bacterial clade

Members of the Bacteria comprising a distinct family within the Alphaproteobacteria that are abundant and ubiquitous in marine environments, and have important roles as oligotrophic heterotrophs.

Mosaic genomes

Genomes assembled from metagenome data that are typically incomplete, in comparison to closed or draft genomes of individual cultivated laboratory-grown isolates.

Phylotypes

Genetic variants of a specific lineage, often used to describe subtypes of a species: for example, an operationally defined measure of phylogenetic clustering of small subunit rRNA (SSU rRNA) gene sequences or internal transcribed spacer sequences of SSU rRNA genes.

Aeolian dispersal

Movement and successful establishment of organisms (in this case, microorganisms) from one location to another mediated by the wind.

Meromictic

A stratified lake that contains an upper mixed layer (mixolimnion) that does not mix with the bottom stagnant anoxic layer (monimolimnion) owing to a steep density gradient (for example, pycnocline, oxycline and chemocline) separating the two layers. By contrast, in a monomictic lake, water throughout the lake (top to bottom) mixes once per year.

Microbial populations

The total contingent of one taxon (for example, species) within a microbial community.

Green sulfur bacteria

(GSB). GSB (Chlorobiaceae) are phototrophic primary producers that fix CO2 at low sunlight intensities and have important roles in sulfur cycling by oxidizing reduced forms of sulfur that are often made available in the system by sulfate-reducing bacteria.

Anoxic

An anoxic environment lacks oxygen, such as the bottom waters of a meromictic lake, where oxygen has been depleted and only anaerobic processes occur (for example, methanogenesis).

Biogeochemical cycles

The influences of both biotic and abiotic processes on the inter-conversion of chemical substances, typically cycling chemicals through oxidized and reduced forms.

Haloarchaea

Heterotrophic members of the domain Archaea that require hypersaline conditions for growth.

Benthic

Benthic organisms live at the bottom of a water body (for example, a lake or an ocean); these include microorganisms growing in mats on the sediment surface and within the shallow subsurface.

Ecotype

A phylotype where the genetic variation manifests in a phenotypic distinction that enables colonization of a specific ecological niche.

Sympatric speciation

The process leading to the evolution of new species from a single ancestral species while inhabiting the same geographic location.

Limnology

The study of inland aquatic (freshwater or saline) systems, including their physical, geological, chemical and biological characteristics.

Virophages

Small viruses that are deleterious to other larger viruses, but also require the larger viruses for their own propagation (for example, by gaining entry to a host cell).

Open discovery

As opposed to the testing of a specific hypothesis, open discovery involves learning something new from data acquired by observation and analysis (for example, metagenome data) that is essentially unforeseeable and is often serendipitous, akin to turning over a rock to discover what lies beneath it, opening an ancient tomb to learn what secrets it holds or viewing a new world for the first time.

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Cavicchioli, R. Microbial ecology of Antarctic aquatic systems. Nat Rev Microbiol 13, 691–706 (2015). https://doi.org/10.1038/nrmicro3549

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