Limitation of bacterial growth by dissolved organic matter in the subarctic Pacific

Kirchman, DL

doi:10.3354/meps062047

Cited by 197 publications

(173 citation statements)

References 20 publications

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“…All cyanobacterial genomes clustered within the oligotrophs, with the open-ocean organisms (Prochlorococcus marinus) displaying more oligotrophic characteristics than those from freshwater (Nostoc and Anabaena). This distinction within the cyanobacteria is consistent with the inception of photosynthesis being associated with adaptation to environments deficient in carbon and energy (23); such conditions pervade in the bulk nutrientdepleted conditions of the open ocean where P. marinus resides (24). Planctomycetes, a group known to become dominant during phytoplankton blooms (25), also belonged to the cluster with Nostoc and Anabaena.…”

Section: Predicting the Lifestyle Of A Bacterium From Genome Sequencementioning

confidence: 67%

The genomic basis of trophic strategy in marine bacteria

Lauro

McDougald

Thomas

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

648

682

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Many marine bacteria have evolved to grow optimally at either high (copiotrophic) or low (oligotrophic) nutrient concentrations, enabling different species to colonize distinct trophic habitats in the oceans. Here, we compare the genome sequences of two bacteria, Photobacterium angustum S14 and Sphingopyxis alaskensis RB2256, that serve as useful model organisms for copiotrophic and oligotrophic modes of life and specifically relate the genomic features to trophic strategy for these organisms and define their molecular mechanisms of adaptation. We developed a model for predicting trophic lifestyle from genome sequence data and tested >400,000 proteins representing >500 million nucleotides of sequence data from 126 genome sequences with metagenome data of whole environmental samples. When applied to available oceanic metagenome data (e.g., the Global Ocean Survey data) the model demonstrated that oligotrophs, and not the more readily isolatable copiotrophs, dominate the ocean's free-living microbial populations. Using our model, it is now possible to define the types of bacteria that specific ocean niches are capable of sustaining.microbial adaptation and ecology ͉ microbial genomics and metagenomics ͉ monitoring environmental health ͉ trophic adaptation T he marine environment is the largest habitat on Earth, accounting for Ͼ90% of the biosphere by volume and harboring microorganisms responsible for Ϸ50% of total global primary production. Within this environment, marine bacteria (and archaea) play a pivotal role in biogeochemical cycles while constantly assimilating, storing, transforming, exporting, and remineralizing the largest pool of organic carbon on the planet (1).Nutrient levels in pelagic waters are not uniform. Large expanses of water are relatively nutrient depleted (e.g., oligotrophic open ocean water), whereas other zones are relatively nutrient rich (e.g., copiotrophic coastal and estuarine waters). Local variations in nutrient content can occur because of physical processes, including upwelling of nutrient rich deep waters or aeolian and riverine deposition, or biological processes such as phytoplankton blooms or aggregation of particulate organic matter. In addition, heterogeneity in ocean waters is not limited to gross differences in nutrient concentrations, but extends to microscale patchiness that occurs throughout the continuum of ocean nutrient concentrations (2).In ecological terms, bacteria are generally defined as rstrategists, having a small body, short generation time, and highly dispersible offspring. Although this strategy is broadly true compared with macroorganisms, bacteria have evolved a wide range of growth and survival strategies to maximize reproductive success. In particular, nutrient type and availability have provided strong selective pressure for defining lifestyle strategies among marine bacteria. However, although a large number of copiotrophic marine organisms (and fewer oligotrophs) have been cultured, the study of trophic strategy has been impaired by a lack of unders...

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Section: Predicting the Lifestyle Of A Bacterium From Genome Sequencementioning

confidence: 67%

The genomic basis of trophic strategy in marine bacteria

Lauro

McDougald

Thomas

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

648

682

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“…The problem with the nitrogen hypothesis, however, is that heterotrophic bacterial production in equatorial waters (Kirchman and Rich in press) and in at least some other open oceanic regions (Kirchman 1990) seems to be limited by carbon, not nitrogen, and so one would expect sugars to limit DIN uptake, not DIN to limit sugar uptake (Kirchman et al 1990). …”

Section: Discussionmentioning

confidence: 99%

“…Bacterial production and growth efficiency can be used to estimate the flux of labile DOM because heterotrophic bacteria are the main sinks of DOM and direct use of particulate organic matter is very low relative to DOM, especially in coastal and oceanic environments (Kirchman 1993). Even though the ratio of bacterial production to primary production (BP:PP) is low in equatorial Pacific waters (-0.15 vs. the average of 0.30 for aquatic systems; Cole et al 1988; see also Ducklow and Carlson 1992), the labile DOM flux in these waters could still be substantial Carlson and Ducklow 1995) and perhaps is even greater north and south of the equator (Kirchman et al 1995).…”

Section: Discussionmentioning

confidence: 99%

“…Burney (1986) used the MBTH method and observed large changes in sugar concentrations over time, suggestive of high fluxes. Kirchman et al (1990) hypothesized that uptake of dissolved inorganic nitrogen (DIN) (principally NH,+ ) by heterotrophic bacteria is driven by monosaccharide uptake, but it is difficult to extrapolate from their enrich-ment experiments to in situ processes. Finally, although they did not measure fluxes, Pakulski and Benner (1994) did find high concentrations of mono-and polysaccharides in equatorial Pacific waters.…”

Section: Acknowledgmentsmentioning

confidence: 99%

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Concentrations and uptake of neutral monosaccharides along 14°W in the equatorial Pacific: Contribution of glucose to heterotrophic bacterial activity and the DOM flux

Rich

Ducklow²,

Kirchman

1996

Limnology & Oceanography

162

168

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We examined concentrations and uptake of dissolved neutral monosaccharides (DNMS) in order to determine the contribution of DNMS to heterotrophic bacterial production and to the flux of dissolved organic matler (DOM) in the equatorial Pacific. DNMS concentrations were greater during El Nifio-affected months of February-April 1992 than during August-October 1992; in contrast, glucose turnover was the oppositeturnover was faster in August-October than in February-April. The variation in sugar concentrations and turnover probably resulted from El Nifio-induced changes in primary production; as El Nifio waned primary production increased, which appeared to stimulate bacterial activity, especially glucose turnover, that in turn forced down DNMS concentrations. In all months, however, DNMS concentrations were low, especially com:pared with total dissolved organic carbon concentrations (< 1%). Glucose was the dominant neutral monosaccharide and alone supported 15-47% of bacterial production. Other monosaccharides apparently did not support much bacterial growth; concentrations of other sugars were low, as probably was turnover. Respiration of glucose (30-60% of uptake) and mannose (60-90%) was relatively high, suggesting that DNMS supported a large fraction of bacterial respiration as well as biomass production. These results point to the importance of DNMS and glucose in particular in supporting bacterial growth and in contributing to the flux #of labile DOM.The concentration of labile dissolved organic matter (DOM) in aquatic ecosystems is usually low, but rates of bacterial activity and biomass production (Cole et al. 1988;Ducklow and Carlson 1992) indicate that DOM fluxes can be quite high. In spite of the recognized importance of DOM, we have few direct measures of DOM fluxes and know little about the composition and uptake of specific components of&e labile DOM pool. Nearly all previous studies on labile DOM have focused on dissolved free amino acids (DFAA) and on the support of bacterial production by DFAA.Free amino acids can provide much C and N for bacterial growth, which in turn suggests that the DFAA is a large component of the labile DOM flux in at least some marine environments. In estuaries, DFAA seems to support a large fraction (if not all) of bacterial production (Billen and Fontigny 1987; Jorgensen et al. 1993;Hoch and Kirchman 1995). Dissolved combined amino acids ' Corresponding author. AcknowledgmentsWe thank R. Penner for his comments about the manuscript.

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“…Numerous studies show bacterial production is carbon limited, even though DOC concentrations are high throughout the water column (Kirchman, 1990;Carlson and Ducklow, 1995;Cherrier et al, 1996;Kirchman and Rich, 1997;Kirchman, 2000). The large reservoir of DOC that accumulates in seawater is therefore believed to be largely unavailable to meet bacterial carbon demand (Kirchman et al, 1993;Carlson and Ducklow, 1995).…”

Section: Introductionmentioning

confidence: 99%

Seqestration of dissolved organic carbon in the deep sea

Repeta¹

2006

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We used compound specific natural abundance radiocarbon analyses of neutral sugars to study carbon cycling of high molecular weight (HMW) dissolved organic carbon (DOC) at two sites in the North Pacific Ocean. Sugars released from HMWDOC by acid hydrolysis were purified by high-pressure liquid chromatography and analyzed for radiocarbon content via accelerator mass spectrometry. We find the seven most

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Limitation of bacterial growth by dissolved organic matter in the subarctic Pacific

Cited by 197 publications

References 20 publications

The genomic basis of trophic strategy in marine bacteria

The genomic basis of trophic strategy in marine bacteria

Concentrations and uptake of neutral monosaccharides along 14°W in the equatorial Pacific: Contribution of glucose to heterotrophic bacterial activity and the DOM flux

Seqestration of dissolved organic carbon in the deep sea

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