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Microbial growth in the polar oceans — role of temperature and potential impact of climate change

Key Points

  • Heterotrophic bacteria and other heterotrophic microorganisms typically process about half of the primary production in the oceans and therefore are important in determining the response of oceanic ecosystems and the carbon cycle to climate change.

  • Previous studies suggested that heterotrophic bacteria are less active and are less important in the carbon cycle in polar waters because of low temperatures.

  • A synthesis of old and new data confirms that the amount of primary production used by heterotrophic bacteria is in fact lower in the Arctic Ocean and in the Ross Sea, Antarctica, than in several lower-latitude oceans.

  • The low rates are not due, however, to low temperatures, but rather to low supply of labile dissolved organic material. Only about 20% of the variation in bacterial growth rates in polar waters can be explained by temperature alone.

  • These results have several implications for understanding how the Arctic Ocean and Antarctic seas may respond to climate changes already affecting these ecosystems. The decline in sea ice cover, for example, is likely to have large effects on ocean mixing and thus the supply of labile organic matter and nutrients supporting bacteria and other microorganisms at the base of polar food chains.

Abstract

Heterotrophic bacteria are the most abundant organisms on the planet and dominate oceanic biogeochemical cycles, including that of carbon. Their role in polar waters has been enigmatic, however, because of conflicting reports about how temperature and the supply of organic carbon control bacterial growth. In this Analysis article, we attempt to resolve this controversy by reviewing previous reports in light of new data on microbial processes in the western Arctic Ocean and by comparing polar waters with low-latitude oceans. Understanding the regulation of in situ microbial activity may help us understand the response of the Arctic Ocean and Antarctic coastal waters over the coming decades as they warm and ice coverage declines.

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Figure 1: Schematic of the microbial loop.
Figure 2: Box and whisker plot of biomass production integrated through the euphotic zone in six regions.
Figure 3: Effect of temperature on the bacterial production to primary production ratio and the bacterial growth rate.
Figure 4: Bacterial growth rate as a function of semi-labile DOC concentrations.
Figure 5: Box and whisker plot of bacterial biomass integrated through the euphotic zone in six regions.
Figure 6: Possible responses in the oceanic microbial food web and fluxes owing to climate change in polar systems.

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Acknowledgements

We thank L. Codispoti for insights and discussion on Arctic biogeochemistry and D. Miller for help with the statistical analyses. This work was supported by NSF OPP 0806295 MEC (to D.L.K.), NSF OPP 0217282 (to H.D.) and a Spanish researcher mobility fellowship (to X.A.G.M.).

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Correspondence to David L. Kirchman.

Supplementary information

Supplementary information S1 (table) | Summary of marine regions and data sets analyzed by this study (PDF 173 kb)

Supplementary information S2 (box) | Methodology (PDF 222 kb)

41579_2009_BFnrmicro2115_MOESM3_ESM.pdf

Supplementary information S3 (figure) | Principal component analysis of abiotic properties of the six oceans examined here. (PDF 334 kb)

41579_2009_BFnrmicro2115_MOESM4_ESM.pdf

Supplementary information S4 (figure) | Ratio of bacterial production to primary production (BP:PP) for the six marine regions. (PDF 218 kb)

41579_2009_BFnrmicro2115_MOESM5_ESM.pdf

Supplementary information S5 (figure) | Bacterial production versus temperature for the six marine regions. (PDF 344 kb)

Supplementary information S6 (figure) | Integrated phytoplankton biomass for the six marine regions. (PDF 212 kb)

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Glossary

Heterotrophic

The use of organic material to supply energy and carbon for synthesis of cellular components.

Marine food web

A term used to refer to the complex suite of predatorprey interactions among organisms in the ocean.

Protist

A single-cell eukaryote, sometimes referred to as a protozoan.

Primary production

The rate at which plant biomass is produced. The estimates discussed here were derived using the 14C method, meaning that the rates are somewhere between gross primary production (without subtracting any loss owing to respiration) and net primary production (for which respiration is considered).

Bacterial production

Analogous to primary production, bacterial production is the rate at which bacterial biomass is produced in the absence of mortality.

Uncoupling

Bacteria are coupled to phytoplankton if their production or biomass levels co-vary over time and space and if correlations between the two are strong regardless of the magnitude of the production or biomass ratios.

Bacterial growth efficiency

The ratio of carbon used for biomass synthesis to total carbon use (synthesis and respiration). In addition to being a crucial parameter in bacterial energetics, bacterial growth efficiency is important in determining how much carbon taken up by bacteria is passed on to higher trophic levels versus that lost to respiration.

Correlation analysis

A method for examining whether two factors co-occur (r = 1, if they do so perfectly, whereas r = −1, if they vary inversely to each other) that is often used in field studies to explore possible causal relationships that cannot be examined by direct experimentation.

Euphotic zone

The upper sunlit layer of the ocean, which extends down to a depth where light is 1% of the surface intensity.

Q10

The factor by which a rate increases after a 10 C increase in temperature. Many biological reactions have a Q10 of 2, which is roughly equivalent to an activation energy of 50 kJ mol1 at 20 oC.

Semi-labile DOC

One simple model of oceanic DOC divides it into three parts: the labile fraction used by bacteria on the day to week timescale; the refractory fraction that bacteria need from years to millennia to degrade; and the semi-labile fraction that is used on timescales between the extremes set by the other two DOC parts. Because labile DOC concentrations are trivial, the size of the semi-labile DOC pool in surface waters can be estimated from the difference between total DOC and deep-water DOC concentrations. DOC at depths below about 1,000 m is refractory and has turnover times that exceed 1,000 years.

Top-down

Top-down factors, such as grazing and viral lysis, affect biomass levels, whereas bottom-up factors, such as temperature and nutrient concentrations, control growth rates.

Bacteriovore

Any organism that eats bacteria. In lakes and the oceans, bacterivores are mostly protists.

Benthos

The community of organisms that live at the sea floor.

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Kirchman, D., Morán, X. & Ducklow, H. Microbial growth in the polar oceans — role of temperature and potential impact of climate change. Nat Rev Microbiol 7, 451–459 (2009). https://doi.org/10.1038/nrmicro2115

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