Different coupling of dissolved amino acid, protein, and carbohydrate turnover to heterotrophic picoplankton production in the Southern Ocean in austral summer and fall

Simon, Meinhard; Rosenstock, Bernd

doi:10.4319/lo.2007.52.1.0085

Cited by 37 publications

(41 citation statements)

References 30 publications

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“…Consistent with our results, gammaproteobacteria take up protein and algal extracts more than other types of DOM in waters of the North Atlantic Ocean and Mediterranean Sea (18,19). Our results suggest a possible switch to protein use in summer when the input of dissolved protein is high coupled to the high phytoplankton biomass typical of these waters in summer (35,40,41). We expected similar results for Ant4D3 and Arctic96B-16 clades because their growth-related activity was similar in WAP waters (12) and because they are closely related (29).…”

Section: Discussionsupporting

confidence: 81%

“…The four LMW compounds examined in the present study were chosen for single-cell analyses because previous reports had found wide variation in total uptake, similar to our results. For example, other studies also found high assimilation of amino acid mixtures (5,35,36). Amino acids may be preferred over other LMW compounds because they fulfill requirements for both nitrogen and carbon (36).…”

Section: Discussionmentioning

confidence: 99%

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Uptake of Dissolved Organic Carbon by Gammaproteobacterial Subgroups in Coastal Waters of the West Antarctic Peninsula

Nikrad

Cottrell

Kirchman

2014

Appl Environ Microbiol

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Heterotrophic bacteria are well known to be key players in the turnover of dissolved organic material (DOM) in the oceans, but the relationship between DOM uptake and bacterial clades is still not well understood. Here we explore the turnover and singlecell use of glucose, an amino acid mixture, N-acetylglucosamine (NAG), and protein by gammaproteobacterial clades in coastal waters of the West Antarctic Peninsula in summer and fall. More than 60% of the cells within two closely related gammaproteobacterial clades, Ant4D3 and Arctic96B-16, were active in using the amino acid mixture, protein, and NAG. In contrast, an average of only 7% of all SAR86 cells used amino acids and protein even in summer when DOM use was high. In addition to DOM uptake within a group, we explored the contribution of the three gammaproteobacterial groups to total community uptake of a compound. SAR86 contributed 5-to 10-fold less than the other gammaproteobacterial subgroups to the uptake of all compounds. We found that the overall contribution of the Ant4D3 clade to DOM uptake was highest, whereas the SAR86 clade contributed the least to DOM turnover in West Antarctic Peninsula waters. Our results suggest that the low growth activity of a bacterial clade leads to low abundance, fewer active cells and a low contribution to the turnover of DOM components.A diverse community of heterotrophic bacteria processes dissolved organic material (DOM) in the Arctic Ocean and Antarctic seas, making up a critical part of the carbon cycle in polar environments. Some members of this community appear to be unique to polar waters, while others are also found in low-latitude oceans (1, 2). Single-cell methods have indicated that these bacteria are active in leucine incorporation (3), even though bulk estimates indicate that DOM fluxes mediated by heterotrophic bacteria are lower in polar waters than in other oceans (4). With few exceptions (5-7), however, previous single-cell studies and the bulk activity studies of polar systems have focused on leucine as a general index of bacterial activity (3,(8)(9)(10)(11)(12)(13). The paucity of data about the uptake of other compounds by specific bacterial taxa hinders efforts to understand mechanisms in bacterial biogeography and the contribution of these bacteria to carbon cycling.Studies examining DOM uptake by gammaproteobacteria, which make up 5 to 25% of the total bacterial community in polar systems and many other oceanic waters (14, 15), provide some examples of differences in the uptake of leucine and other DOM components among bacterial clades. Gammaproteobacteria took up more leucine and an amino acid mixture than ATP or glucose in Mediterranean coastal water according to single-cell studies (16,17). Similarly, in the Arctic Ocean, gammaproteobacteria preferred amino acids to other types of low-molecular-weight (LMW) DOM, such as ATP or glucose (5, 6). However, the uptake of protein, algal derivatives, extracellular polysaccharides, and chitin by gammaproteobacteria was higher than their affinity for LMW...

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Section: Discussionsupporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

Uptake of Dissolved Organic Carbon by Gammaproteobacterial Subgroups in Coastal Waters of the West Antarctic Peninsula

Nikrad

Cottrell

Kirchman

2014

Appl Environ Microbiol

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“…The applied electrospray ionization in negative mode potentially adds a further bias constraining our analytical window Herlemann et al, 2014). Nevertheless, our analysis did well in recovering fractions of highly unsaturated aliphatic molecules and some carbohydrates that both significantly increased with marine influence, and our statistics revealed that the abundance of some active OTUs (RNA-based) is related to potentially easily degradable compounds such as peptides (for example, Keil and Kirchman, 1999;Simon and Rosenstock, 2007;Figure 6b). Free and total dissolved neutral sugars were related to the salinity gradient, but did not show significant correlations to DOM, active or total community composition (Supplementary Table S5).…”

Section: Identifying the Key Factors-dom Moleculesmentioning

confidence: 93%

“…It is important to emphasize that turnover rate and concentration of a substrate compound are often inversely related such as for dissolved carbohydrates (Simon and Rosenstock, 2007). A highly labile substrate to which bacteria have a high affinity can reach steady-state equilibrium concentrations below detection limit, although production and consumption rates are high.…”

Section: Identifying the Key Factors-dom Moleculesmentioning

confidence: 99%

“…In addition, solid-phase extraction of the samples with an efficiency of~52% on a carbon basis may not have representatively captured the most labile components of the DOM such as amino acids, DNA-based unrooted tree DOM-bacteria associations in the North Sea H Osterholz et al peptides, mono-and polysaccharides (Hertkorn et al, 2013;Osterholz et al, 2015), which are rapidly turned over by the diverse, active BC (Simon and Rosenstock, 2007;Zubkov et al, 2008). The applied electrospray ionization in negative mode potentially adds a further bias constraining our analytical window Herlemann et al, 2014).…”

Section: Identifying the Key Factors-dom Moleculesmentioning

confidence: 99%

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Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system

et al. 2016

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Dissolved organic matter (DOM) is the main substrate and energy source for heterotrophic bacterioplankton. To understand the interactions between DOM and the bacterial community (BC), it is important to identify the key factors on both sides in detail, chemically distinct moieties in DOM and the various bacterial taxa. Next-generation sequencing facilitates the classification of millions of reads of environmental DNA and RNA amplicons and ultrahigh-resolution mass spectrometry yields up to 10 000 DOM molecular formulae in a marine water sample. Linking this detailed biological and chemical information is a crucial first step toward a mechanistic understanding of the role of microorganisms in the marine carbon cycle. In this study, we interpreted the complex microbiological and molecular information via a novel combination of multivariate statistics. We were able to reveal distinct relationships between the key factors of organic matter cycling along a latitudinal transect across the North Sea. Total BC and DOM composition were mainly driven by mixing of distinct water masses and presumably retain their respective terrigenous imprint on similar timescales on their way through the North Sea. The active microbial community, however, was rather influenced by local events and correlated with specific DOM molecular formulae indicative of compounds that are easily degradable. These trends were most pronounced on the highest resolved level, that is, operationally defined 'species', reflecting the functional diversity of microorganisms at high taxonomic resolution.

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Crustacean zooplankton release copious amounts of dissolved organic matter as taurine in the ocean

Clifford

Hansell

Varela

et al. 2017

Limnology & Oceanography

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Taurine (Tau), an amino acid‐like compound, is present in almost all marine metazoans including crustacean zooplankton. It plays an important physiological role in these organisms and is released into the ambient water throughout their life cycle. However, limited information is available on the release rates by marine organisms, the concentrations and turnover of Tau in the ocean. We determined dissolved free Tau concentrations throughout the water column and its release by abundant crustacean mesozooplankton at two open ocean sites (Gulf of Alaska and North Atlantic). At both locations, the concentrations of dissolved free Tau were in the low nM range (up to 15.7 nM) in epipelagic waters, declining sharply in the mesopelagic to about 0.2 nM and remaining fairly stable throughout the bathypelagic waters. Pacific amphipod–copepod assemblages exhibited lower dissolved free Tau release rates per unit biomass (0.8 ± 0.4 μmol g−1 C‐biomass h−1) than Atlantic copepods (ranging between 1.3 ± 0.4 μmol g−1 C‐biomass h−1 and 9.5 ± 2.1 μmol g−1 C‐biomass h−1), in agreement with the well‐documented inverse relationship between biomass‐normalized excretion rates and body size. Our results indicate that crustacean zooplankton might contribute significantly to the dissolved organic matter flux in marine ecosystems via dissolved free Tau release. Based on the release rates and assuming steady state dissolved free Tau concentrations, turnover times of dissolved free Tau range from 0.05 d to 2.3 d in the upper water column and are therefore similar to those of dissolved free amino acids. This rapid turnover indicates that dissolved free Tau is efficiently consumed in oceanic waters, most likely by heterotrophic bacteria.

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Different coupling of dissolved amino acid, protein, and carbohydrate turnover to heterotrophic picoplankton production in the Southern Ocean in austral summer and fall

Cited by 37 publications

References 30 publications

Uptake of Dissolved Organic Carbon by Gammaproteobacterial Subgroups in Coastal Waters of the West Antarctic Peninsula

Uptake of Dissolved Organic Carbon by Gammaproteobacterial Subgroups in Coastal Waters of the West Antarctic Peninsula

Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system

Crustacean zooplankton release copious amounts of dissolved organic matter as taurine in the ocean

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