Abstract
Marine bacteria drive the biogeochemical processing of oceanic dissolved organic carbon (DOC), a 750-Tg C reservoir that is a critical component of the global C cycle. Catabolism of DOC is thought to be regulated by the biomass composition of heterotrophic bacteria, as cells maintain a C:N:P ratio of ∼50:10:1 during DOC processing. Yet a complicating factor in stoichiometry-based analyses is that bacteria can change the C:N:P ratio of their biomass in response to resource composition. We investigated the physiological mechanisms of resource-driven shifts in biomass stoichiometry in continuous cultures of the marine heterotrophic bacterium Ruegeria pomeroyi (a member of the Roseobacter clade) under four element limitation regimes (C, N, P, and S). Microarray analysis indicated that the bacterium scavenged for alternate sources of the scarce element when cells were C-, N-, or P-limited; reworked the ratios of biomolecules when C- and P- limited; and exerted tighter control over import/export and cytoplasmic pools when N-limited. Under S limitation, a scenario not existing naturally for surface ocean microbes, stress responses dominated transcriptional changes. Resource-driven changes in C:N ratios of up to 2.5-fold and in C:P ratios of up to sixfold were measured in R. pomeroyi biomass. These changes were best explained if the C and P content of the cells was flexible in the face of shifting resources but N content was not, achieved through the net balance of different transcriptional strategies. The cellular-level metabolic trade-offs that govern biomass stoichiometry in R. pomeroyi may have implications for global carbon cycling if extendable to other heterotrophic bacteria. Strong homeostatic responses to N limitation by marine bacteria would intensify competition with autotrophs. Modification of cellular inventories in C- and P-limited heterotrophs would vary the elemental ratio of particulate organic matter sequestered in the deep ocean.
Highlights
Bacterioplankton control the flux of dissolved organic carbon (DOC) into the microbial food web and influence the release of carbon to atmospheric, offshore, and deep sea reservoirs
We investigated the physiological mechanisms of resource-driven shifts in biomass stoichiometry in continuous cultures of the marine heterotrophic bacterium Ruegeria pomeroyi under four element limitation regimes (C, N, P, and S)
Resource-driven shifts in C:N:P ratios of bacterial biomass can affect the efficiency of DOC transformation, modify C flux through the marine food web (Elser et al, 1995), buffer mismatches between bacterial requirements and ecosystem resource availability, and alter the composition of particulate organic matter sequestered in the deep ocean (Thingstad et al, 2008)
Summary
Bacterioplankton control the flux of dissolved organic carbon (DOC) into the microbial food web and influence the release of carbon to atmospheric, offshore, and deep sea reservoirs. A confounding factor in stoichiometry-based analyses is that heterotrophic bacteria can change the C:N:P ratio of their biomass in response to the substrate composition (Martinussen and Thingstad, 1987; Tezuka, 1990; Fagerbakke et al, 1996; Gundersen et al, 2002). This plasticity occurs either by uncoupling catabolism and anabolism to overproduce metabolites rich in the excess element (which can be stored or excreted), or by reducing the requirement for the limiting element. Resource-driven shifts in C:N:P ratios of bacterial biomass can affect the efficiency of DOC transformation, modify C flux through the marine food web (Elser et al, 1995), buffer mismatches between bacterial requirements and ecosystem resource availability, and alter the composition of particulate organic matter sequestered in the deep ocean (Thingstad et al, 2008)
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