tmp7066 TMP

Microbial Heterotrophic
Metabolic Rates Constrain the

Microbial Carbon Pump
Carol Robinson1* and Nagappa Ramaiah2
The respiration of dissolved organic matter by heterotrophic bacteria and Archaea represents the largest sink in the global marine biological
carbon cycle, an important constraint on organic carbon supply, and the major driver of global elemental nutrient cycles. Direct measurement
of heterotrophic production and respiration is difficult. However, the recent development of methods involving in vivo electron transport
system activity, bioassay uptake of specific prokaryotic substrates, and nutrient addition incubations are poised to discern the complex
interactions between metabolic rate, community structure, and organic and inorganic nutrient availability. In a changing global environment,
it is important to understand how increasing sea surface temperature, melting sea ice, ocean acidification, variable dust deposition, and
upwelling intensity will impact the metabolism of Bacteria and Archaea and so the balance between carbon sequestration and carbon
dioxide evasion to the atmosphere. Continued and improved measures of prokaryotic production and respiration are vital components of
this endeavor.
he downward flux of organic carbon from the surface ocean to

depth via passive sinking of particles, active transport by animals, and mixing of dissolved organic matter (DOM) is known as
the biological carbon pump (BCP). The microbial carbon pump (MCP)
is a conceptual component of the BCP, used to describe the microbial
production of refractory DOM (RDOM) which can be stored for millennia in the deep sea, rather than being respired to dissolved inorganic
carbon and returned to the atmosphere (1). Heterotrophic bacteria and
Archaea generate RDOM through degradation and transformation of
particulate and dissolved organic matter, exudation, and cell lysis (2,
3). In addition to assimilation and transformation of recently produced
DOM, prokaryotes also degrade older DOM (4) derived from photochemically transformed upwelled DOM (5, 6) and potentially from
methane seeps (7). Hence, understanding the magnitude and variability of the production and respiration of bacteria and Archaea is important not only for quantifying the efficiency of the BCP (8) and the role
of prokaryotes in regulating carbon fluxes (9), but also for constraining
the flow of DOM through the MCP.
The composition and lability of DOM affect the prokaryotic carbon
demand [PrCD = prokaryotic production (PrP) + prokaryotic respiration (PrR)] and the prokaryotic growth efficiency (PrGE = PrP/PrCD,
the proportion of the prokaryotic carbon demand used for prokaryotic
production). PrGE is influenced by the availability of organic and inorganic substrates as well as the energetic costs of growth in a particular
environment, and so tends to be low at times of nutrient limitation or
environmental stress and higher during increased primary productivity
and supply of nutrients (8, 10).
The direct measurement of PrP and PrR and calculation of PrCD
and PrGE is technically and interpretatively challenging. This is due to
uncertainties associated with factors such as the pre-incubation separation of the heterotrophic bacterioplankton fraction from the rest of
the plankton community, the different incubation times required for
PrR and PrP measurements, the effect of light on PrP and PrR, the
quantification of prokaryotic excretion of DOM, and the conversion
factors used to derive rates of carbon production and respiration from
radiolabeled thymidine or leucine incorporation and oxygen consumption (8,9). Large uncertainties in PrGE contribute significantly to the
School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, U.K.
National Institute of Oceanography, Dona Paula 403004, Goa, India
*To whom correspondence should be addressed. E-mail: [email protected]
2
52
mismatch between measurements of mesopelagic microbial metabolic

activity and estimates of the influx of organic carbon that could support this microbial activity (11).
Recent methodological developments have the potential to reduce
uncertainties in PrR and PrP determinations. For example, measurements of in vivo electron transport system activity estimated from the
reduction of the tetrazolium salt INT are linearly related to in situ rates
of respiration, and avoid problems associated with pre-incubation filtration and relatively long incubation times (24 hours) (12). Additionally, single cell assays that measure incorporation of selected organic
compounds by specific prokaryotic groups compare and contrast the
components of DOM taken up by bacteria and Archaea (13). Including these assays in time series studies can elucidate the influence of
environmental factors such as light on PrP (14, 15).
Climate change will likely affect precipitation, river flow, ice
melt, atmospheric deposition, and the timing and strength of alongshore winds that stimulate coastal upwelling, and so may significantly
change the supply of inorganic and organic substrates to marine prokaryotes. Concomitant increases in sea surface temperature and decreases in pH and carbonate ion concentration could lead to changes
in phytoplankton and zooplankton community structure, subsequently
impacting foodweb-derived DOC (16). In short-term experiments,
prokaryotic turnover of phytoplankton-derived polysaccharides was
increased at the lower pH levels projected to occur with a doubling of
atmospheric CO2, with the potential to reduce carbon export and enhance respiratory CO2 production (17). Field studies and inorganic and
organic nutrient bioassay experiments show PrR and PrGE in coastal
regions to be either mainly controlled by the DOC pool or colimited by
organic and inorganic nutrients (1820). Climate-driven increases in
DOC supply may also impact the plankton community photosynthesis
to respiration (P:R) ratio. When released from organic carbon limitation, heterotrophic prokaryotes can outcompete phytoplankton for inorganic nutrients, thereby decreasing the overall P:R ratio, increasing
the proportion of DOC that is respired, and decreasing the amount that
is sequestered (21).
This review aims to highlight our incomplete understanding for the
causes of variability in the PrGE and respiratory potential of heterotrophic bacteria and Archaea. As new research supports the pivotal role
of these microbes in the present and future ocean (22, 23), the lack
of routine measurements of PrP and PrR in relation to phylogenetic
composition, as well as to DOM characterization and assimilation potential, becomes increasingly difficult to defend.
References and Notes

1. N. Jiao et al., Nature Rev. Microbiol. 8, 593 (2010).
2. T. Nagata, in Microbial Ecology of the Oceans D.L. Kirchman Ed. (John
Wiley & Sons, Inc. New York, ed. 1. 2000), pp. 121152.
3. D. F. Gruber, J. P. Simjouw, S. P. Seitzinger, and G. L. Taghon, Appl. Environ.
Microbiol. 72, 4184 (2006).
4. J. Cherrier, J. E. Bauer, E. R. M. Druffel, R. B. Coffin, J. P. Chanton, Limnol.
Oceanogr. 44, 730 (1999).
5. R. Benner, B. Biddanda, Limnol. Oceanogr. 43, 1373 (1998).
6. I. Obernosterer, B. Reitner, G. J. Herndl, Limnol. Oceanogr. 44, 1645 (1999).
7. J. W. Pohlman, J. E. Bauer, W. F. Waite, C. L. Osburn, N. R. Chapman, Nature
Geosci. 4, 37 (2011).
8. C. Robinson, in Microbial Ecology of the Oceans D.L. Kirchman Ed. (John
Wiley & Sons, Inc. ed. 2. 2008), pp. 299334.
9. J. M. Gasol et al., Aquat. Microb. Ecol. 53, 21 (2008).
10. P. A. del Giorgio, J. J. Cole, in Microbial Ecology of the Oceans D. L.
Kirchman Ed. (John Wiley & Sons, Inc. New York ed. 1. 2000), pp. 289325.
11. A. B. Burd et al., Deep Sea Res. II 57, 1557 (2010).
12. S. Martinez-Garca, E. Fernndez, M. Aranguren-Gassis, E. Teira, Limnol.
Oceanogr. Methods 7, 459 (2009).
13. D.L. Kirchman, H. Elifantz, A. I. Dittel, R. R. Malmstrom, M. T. Cottrell,

Limnol. Oceanogr. 52, 495 (2007).
14. M. J. Church, H. W. Ducklow, D.A. Karl, Appl. Environ. Microbiol. 70, 4079
(2004).
15. T. R. A. Straza, D. L. Kirchman, Aquat. Microb. Ecol. 62, 267(2011).
16. O. Hoegh-Guldberg, J. F. Bruno, Science 328, 1523 (2010).
17. J. Piontek, M. Lunau, N. Handel, C. Borchard, M. Wurst, A. Engel,
Biogeosciences 7, 1615 (2010).
18. J. K. Apple, P.A. del Giorgio, ISME J. 1, 729 (2007).
19. L. Alonso-Sez et al., Limnol. Oceanogr. 52, 533 (2007).
20. S. Martinez-Garca et al., Aquat. Microb. Ecol. 416, 17 (2010).
21. T. F. Thingstad et al., Nature 455, 387 (2008).
22. J. Arstegui, J. M. Gasol, C. M. Duarte, G. J. Herndl, Limnol. Oceanogr. 54,
1501 (2009).
23. D. L. Kirchman, X. A. G. Moran, H. W. Ducklow, Nature Rev. Microbiol. 7,
451 (2009).
24. This work was supported by the Scientific Committee on Oceanic
Research (WG134), The Royal Society, and the National Institute of
Oceanography.
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Microbial Heterotrophic

Metabolic Rates Constrain the

he downward flux of organic carbon from the surface ocean to

mismatch between measurements of mesopelagic microbial metabolic

References and Notes

13. D.L. Kirchman, H. Elifantz, A. I. Dittel, R. R. Malmstrom, M. T. Cottrell,

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