Relations between bacterial nitrogen metabolism and growth efficiency in an estuarine and an open-water ecosystem

Jørgensen, Niels O. G.; Kroer, Niels; Coffin, Richard B.; Hoch, Matthew P.

doi:10.3354/ame018247

Cited by 57 publications

(45 citation statements)

References 41 publications

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“…The C : N s ratio and multiple substrate sources-Our current results confirm our previous conclusions (Goldman and Dennett 1991) and those of Tupas and Koike (1990;1991) that cometabolism of amino acids and NH 4 ϩ is a common occurrence in marine bacteria and that there is absolutely no evidence that NH 4 ϩ uptake is inhibited in the presence of amino acids, as has been suggested previously (Kirchman et al 1989;Kirchman 1994;Jorgensen et al 1999). The key factor regulating the uptake of NH 4 ϩ is the availability of a carbon source to provide a stoichiometric balance between C and N uptake, as regulated by the C : N B ratio and GGE of the bacterial population.…”

Section: Discussionsupporting

confidence: 92%

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

Goldman

Dennett

2000

Limnology & Oceanography

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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.

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Section: Discussionsupporting

confidence: 92%

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

Goldman

Dennett

2000

Limnology & Oceanography

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“…There is presently very little research on variations in BR cell Ϫ1 in either freshwater (Cimbleris and Kalff 1998) or marine waters (Jorgensen et al 1999). However, our results would argue that, while BR may often be rather invariant in aquatic ecosystems, BR cell Ϫ1 is highly variable and perhaps the more appropriate scale when considering how variations in respiration relate to BGE.…”

Section: Discussionmentioning

confidence: 72%

Bacterial metabolism and growth efficiency in lakes: The importance of phosphorus availability

Smith

Prairie

2004

Limnology & Oceanography

195

152

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We investigated bacterial responses to variations in dissolved organic carbon (DOC) and nutrient availability by a comparative analysis of bacterial metabolism in lakes ranging from oligotrophic to eutrophic. Bacterial growth, respiration, and growth efficiency were quantified in lake water dilution cultures performed in 20 lakes located in eastern Quebec, Canada, which varied with respect to both DOC and nutrient concentrations. Intrinsic growth rates of the bacteria ranged from 0.1 to 1.4 d Ϫ1 , bacterial cell-specific respiration rates ranged from 0.4 to 7.2 fg C cell, and growth efficiencies ranged from 6.7% to 51.6%. These variations were unrelated to bulk DOC concentrations. Instead, growth rate and efficiency were positively related to total phosphorus concentrations. Specific respiration rate, on the other hand, decreased with increasing phosphorus concentrations, and the magnitude of respiration, on a per-cell basis, strongly influenced observed growth efficiencies. In a series of substrate enrichment experiments, additions of glucose alone failed to stimulate a response in growth rate, mean cell biovolume, or the potential biomass yield in dilution cultures, but all responded positively to phosphorus additions. Our results show that bacterial metabolism and the fate of DOC input to lake microbial communities are strongly dependent on phosphorus availability, rather than total carbon availability. Extreme oligotrophy appears to place high respiratory demands on the bacterioplankton, resulting in very low bacterial growth efficiencies and consequently greater DOC flow to CO 2 than to biomass available for transfer to higher trophic levels.The organic carbon fueling bacterial metabolism in lakes originates from either in situ primary production (autochthonous carbon) or from terrestrial production that is carried into the lake from its watershed (allochthonous carbon). The relative importance of these two sources of carbon is highly variable among lakes. While autochthonous carbon tends to predominate in very eutrophic lakes, allochthonous carbon loading often greatly exceeds in situ primary production in oligotrophic lakes (Wetzel 1992). Input of allochthonous carbon thus represents a potentially large subsidy to the metabolism of lake communities.Several lines of evidence argue that the total respiratory breakdown of organic matter exceeds that produced by in situ primary production in most lakes (e.g., del Giorgio and Peters 1994;Cole et al. 2000). This metabolic imbalance (net heterotrophy; total respiration Ͼ gross primary production) implies that allochthonous carbon must support a portion of the lake's total respiration. Indeed, it has recently been shown that, based on epilimnetic dissolved oxygen mea-1 To whom correspondence should be addressed. Present address: Department of Biological Sciences, University of South Carolina, Columbia, South Carolina 29208 (smithe@biol.sc.edu). AcknowledgmentsWe thank A. Beauchemin for assistance with field and laboratory sampling; C. Côté for providing n...

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“…In two streams in Sweden, 19 to 55% of the bulk DON was found to be bioavailable in short-term bioassays (Stepanauskas et al, 2000); only 5 to 18% of the DON was identified as urea, DCAA or DFAA indicating that bacteria also utilize additional organic N compounds. In the Gulf of Riga, 13% of the DON was bioavailable during 7 to 8 day bioassay experiments (Jørgensen et al, 1999).…”

Section: Results From Bioassaysmentioning

confidence: 99%

DON as a source of bioavailable nitrogen for phytoplankton

See²,

et al. 2007

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Abstract. Relative to inorganic nitrogen, concentrations of dissolved organic nitrogen (DON) are often high, even in regions believed to be nitrogen-limited. The persistence of these high concentrations led to the view that the DON pool was largely refractory and therefore unimportant to plankton nutrition. Any DON that was utilized was believed to fuel bacterial production. More recent work, however, indicates that fluxes into and out of the DON pool can be large, and that the constancy in concentration is a function of tightly coupled production and consumption processes. Evidence is also accumulating which indicates that phytoplankton, including a number of harmful species, may obtain a substantial part of their nitrogen nutrition from organic compounds. Ongoing research includes ways to discriminate between autotrophic and heterotrophic utilization, as well as a number of mechanisms, such as cell surface enzymes and photochemical decomposition, that could facilitate phytoplankton use of DON components.

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Relations between bacterial nitrogen metabolism and growth efficiency in an estuarine and an open-water ecosystem

Cited by 57 publications

References 41 publications

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

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

Bacterial metabolism and growth efficiency in lakes: The importance of phosphorus availability

DON as a source of bioavailable nitrogen for phytoplankton

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