Growth of marine bacteria in batch and continuous culture under carbon and nitrogen limitation

Abstract

In a combination of batch and continuous culture experiments involving natural assemblages of marine bacteria we examined the impact of varying both the carbon and nitrogen substrates and the substrate C : N ratio (C : N S ) on the bacterial C : N ratio (C : N B ), the gross growth efficiency (GGE), and the ability of marine bacteria to cometabolize amino acids and NH 4 ϩ . We varied the C : N S ratio from 5 : 1 (carbon limitation) to 30 : 1 (nitrogen limitation) with varying combinations of glucose, glutamate, and NH 4 ϩ (and in some cases with an amino acid mixture and with other simple carbon compounds). We found that GGE was unaffected by growth rate, the C : N S ratio, or different combinations of carbon and nitrogen substrates, averaging ϳ50%. However, the 95% confidence interval was as high as Ϯ20%, suggesting that experimental error may be a common problem in determining GGE in laboratory studies and a far more serious problem in making such estimates in field studies. The C : N B ratio was invariant at ϳ4.5 : 1 (by atoms) under all conditions when carbon was limiting growth, but increased to ϳ7 : 1-9 : 1 when reaching the stationary phase during batch growth and up to 13 : 1 at very low growth rates in continuous culture. These results indicate that the C : N B ratio has some value as a diagnostic tool for determining the physiological state of bacterial populations, although there are some concerns about its general applicability. Finally, there was absolutely no evidence that NH 4 ϩ uptake was inhibited in the presence of amino acids. The key to NH 4 ϩ uptake is the presence of a readily assimilated carbon source to balance nitrogen uptake stoichiometrically. These findings have some bearing on the recent suggestions that gradients exist in both GGE and nitrogen preference of marine bacteria from productive inshore regions to the oligotrophic open ocean.

Regulation of growth and energetics of a marine bacterium by nitrogen source and iron availability

“…The energetic costs of using nitrate, which must be reduced to ammonium before use in biosynthesis, seem clearer, although we are not aware of any study examining growth rates of bacteria using nitrate as a nitrogen source. Carbon growth efficiencies are similar when bacteria use glucose plus ammonium or amino acids (Goldman & Dennett 2000), but the impact of nitrate use is not known.…”

“…Growth rates of cultured bacteria are often highest in complex media and in media supplemented by amino acids (Marr 1991), but this organic nitrogen effect was not observed for a mixed culture of marine bacteria (Goldman & Dennett 2000). Growth on amino acids may not be faster if the transport costs of using several amino acids exceed the energetic advantage of avoiding amino acid synthesis, which is necessary for cells growing on ammonium and a suitable carbon source.…”

Emergence in pelagic communities

“…However, there is some doubt about the ease or extent to which bacterial populations exploit the largest pool of organic carbon: bacterial biomass is scarcely correlated to total DOC availability so much as to phytoplankton productivity (Bird and Kalff, 1984). Moreover, on the premise of experiments by Goldman and Dennett (2000), the C:N ratios for oceanic bacterial biomass that are commonly reported (4.5:1 to 7:1; e.g. Kirchman, 1990) rather indicate that natural bacterial growth is limited by the supply of DOC.…”

Coherent patterns in bacterial growth, growth efficiency, and leucine metabolism along a northeastern Pacific inshore‐offshore transect

“…There also appears to be large spatial as well as temporal variability in BGE (Lemée et al 2002;Reinthaler and Herndl 2005;Alonso-Sá ez et al 2007). The low values of oceanic BGE present the problem that, when combined to in situ measurements of BP, they result in estimates of total bacterial carbon consumption that often exceed local and regional estimates of primary production and organic carbon flow (del Giorgio and Cole 2000; Hoppe et al 2006;Carlson et al 2007), thus questioning the robustness of these estimates (Goldman and Dennett 2000). It is then of fundamental importance to better constrain BGE, growth, and C processing by bacteria and assess how the links between them vary across marine environmental gradients.…”