Acetate cycling in the water column of the Cariaco Basin: Seasonal and vertical variability and implication for carbon cycling

Ho, Tung‐Yuan; Scranton, Mary I.; Taylor, Gordon; Varela, Ramón; Thunell, Robert C.; Muller‐Karger, Frank E.

doi:10.4319/lo.2002.47.4.1119

Cited by 83 publications

(59 citation statements)

References 45 publications

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“…The lacking transfer of methane carbon into the assimilatory system may appear counterintuitive. However, autotrophic carbon fixation during growth on organic substrates has been previously demonstrated (36,37). Particularly under the strongly negative redox potentials in sulfidic environments, microorganisms are able to fix inorganic carbon with relatively low input of energy, using the acetyl-CoA pathway (38).…”

Section: Resultsmentioning

confidence: 99%

Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities

Kellermann

Wegener

Elvert

et al. 2012

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

129

141

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The methane-rich, hydrothermally heated sediments of the Guaymas Basin are inhabited by thermophilic microorganisms, including anaerobic methane-oxidizing archaea (mainly ANME-1) and sulfatereducing bacteria (e.g., HotSeep-1 cluster). We studied the microbial carbon flow in ANME-1/ HotSeep-1 enrichments in stable-isotopeprobing experiments with and without methane. The relative incorporation of 13 C from either dissolved inorganic carbon or methane into lipids revealed that methane-oxidizing archaea assimilated primarily inorganic carbon. This assimilation is strongly accelerated in the presence of methane. Experiments with simultaneous amendments of both 13 C-labeled dissolved inorganic carbon and deuterated water provided further insights into production rates of individual lipids derived from members of the methane-oxidizing community as well as their carbon sources used for lipid biosynthesis. In the presence of methane, all prominent lipids carried a dual isotopic signal indicative of their origin from primarily autotrophic microbes. In the absence of methane, archaeal lipid production ceased and bacterial lipid production dropped by 90%; the lipids produced by the residual fraction of the metabolically active bacterial community predominantly carried a heterotrophic signal. Collectively our results strongly suggest that the studied ANME-1 archaea oxidize methane but assimilate inorganic carbon and should thus be classified as methane-oxidizing chemoorganoautotrophs.methanotrophy | biomarker | acetyl-CoA pathway | syntrophy M ethane is an important greenhouse gas and the most abundant hydrocarbon in marine sediments. Its upward flux to the sediment-water interface is strongly reduced by sulfate-dependent anaerobic oxidation of methane (AOM) (1, 2). AOM is performed by syntrophic associations of anaerobic methane-oxidizing archaea (ANMEs) (3, 4) and their sulfate-reducing bacterial partners (SRBs) (mainly relatives of Desulfosarcina or Desulfobulbus) (5-8). The free energy yield of the AOM net reaction is one of the lowest known for catabolic reactions under environmental conditions (ΔG ranges from -20 to -40 kJ·mol -1 ; e.g., refs. 9, 10). Consequently, activity and biomass doubling times determined under optimized laboratory conditions range from 2 to 5 mo (11) and growth yields are extremely low, around 1% relative to oxidized methane (11,12). The biomass of ANMEs and SRBs involved in AOM is usually strongly depleted in 13 C. For instance, at methane seep locations, the δ 13 C values of specific bacterial fatty acids and archaeal ether lipids range from -60 to -100‰ and -70 to -130‰, respectively (e.g., refs. 13-17). Such low values have been interpreted as evidence for the incorporation of 13 C-depleted methane into biomass (e.g., refs. 3, 4, 18).One way to identify the carbon sources of microbial biomass is to perform stable-isotope-probing (SIP) experiments (19), followed by analysis of biomolecules such as membrane lipids (lipid-SIP hereafter). Application of lipid-SIP to cold seep sediments and micro...

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Section: Resultsmentioning

confidence: 99%

Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities

Kellermann

Wegener

Elvert

et al. 2012

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

129

141

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“…Yet past reports based on radioactive substrate additions have unequivocally demonstrated extremely rapid turnover of acetate in oxic environments across fresh and marine surface waters [33][34][35][36] , suggesting active production of acetate from multiple metabolic pathways 37 in oxic environments, as well as very efficient uptake [33][34][35][36] . Fermentative metabolism by diverse and widespread facultative anaerobic bacteria in particle-associated microanoxic zones could be the main source of water column acetate [38][39][40] , and such microhabitats could be directly associated to algae or to particles 19 , yet in vitro work as well as our own results further suggest that methanogenesis proceeds even when these potential sites are removed 18,19 .…”

Section: Discussionmentioning

confidence: 99%

“…The potential importance of acetate for oxic water methanogenesis is intriguing, as acetate concentrations are typically extremely low in oxic surface waters 18,[33][34][35] , and the presence of oxygen may inhibit acetate consumption 27 . Yet past reports based on radioactive substrate additions have unequivocally demonstrated extremely rapid turnover of acetate in oxic environments across fresh and marine surface waters [33][34][35][36] , suggesting active production of acetate from multiple metabolic pathways 37 in oxic environments, as well as very efficient uptake [33][34][35][36] .…”

Section: Discussionmentioning

confidence: 99%

Oxic water column methanogenesis as a major component of aquatic CH4 fluxes

et al. 2014

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Methanogenesis has traditionally been assumed to occur only in anoxic environments, yet there is mounting, albeit indirect, evidence of methane (CH 4 ) production in oxic marine and freshwaters. Here we present the first direct, ecosystem-scale demonstration of methanogenesis in oxic lake waters. This methanogenesis appears to be driven by acetoclastic production, and is closely linked to algal dynamics. We show that oxic water methanogenesis is a significant component of the overall CH 4 budget in a small, shallow lake, and provide evidence that this pathway may be the main CH 4 source in large, deep lakes and open oceans. Our results challenge the current global understanding of aquatic CH 4 dynamics, and suggest a hitherto unestablished link between pelagic CH 4 emissions and surface-water primary production. This link may be particularly sensitive to widespread and increasing human influences on aquatic ecosystem primary productivity.

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“…A volatile degradation product of DMSP (dimethylsulfide [DMS]) escapes to the atmosphere, where it influences climate through cloud formation (1). Bacterial utilization of DMSP is also important and, along with simple sugars, amino acids, and carboxylic acids, can satisfy an important fraction of the bacterial carbon and sulfur demands in various marine environments (13,16,30,37). DMSP has been shown to support up to 13% of the bacterial carbon demand in marine surface waters (16,34) and to provide enough S to satisfy all or most of the requirements of this element for bacterial growth (16,18,34,40).…”

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confidence: 99%

Dimethylsulfoniopropionate Turnover Is Linked to the Composition and Dynamics of the Bacterioplankton Assemblage during a Microcosm Phytoplankton Bloom

Pinhassi¹,

Simó

González

et al. 2005

Appl Environ Microbiol

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Processing of the phytoplankton-derived organic sulfur compound dimethylsulfoniopropionate (DMSP) by bacteria was studied in seawater microcosms in the coastal Gulf of Mexico (Alabama). Modest phytoplankton blooms (peak chlorophyll a [Chl a] concentrations of ϳ2.5 g liter ؊1 ) were induced in nutrient-enriched microcosms, while phytoplankton biomass remained low in unamended controls (Chl a concentrations of ϳ0.34 g liter ؊1 ). Particulate DMSP concentrations reached 96 nM in the enriched microcosms but remained approximately 14 nM in the controls. Bacterial biomass production increased in parallel with the increase in particulate DMSP, and nutrient limitation bioassays in the initial water showed that enrichment with DMSP or glucose caused a similar stimulation of bacterial growth. Concomitantly, increased bacterial consumption rate constants of dissolved DMSP (up to 20 day ؊1 ) and dimethylsulfide (DMS) (up to 6.5 day ؊1 ) were observed. Nevertheless, higher DMSP S assimilation efficiencies and higher contribution of DMSP to bacterial S demand were found in the controls compared to the enriched microcosms. This indicated that marine bacterioplankton may rely more on DMSP as a source of S under oligotrophic conditions than under the senescence phase of phytoplankton blooms. Phylogenetic analysis of the bacterial assemblages in all microcosms showed that the DMSP-rich algal bloom favored the occurrence of various Roseobacter members, flavobacteria (Bacteroidetes phylum), and oligotrophic marine Gammaproteobacteria. Our observations suggest that the composition of the bacterial assemblage and the relative contribution of DMSP to the overall dissolved organic sulfur/organic matter pool control how efficiently bacteria assimilate DMSP S and thereby potentially divert it from DMS production.During blooms of phytoplankton, and particularly during their senescence, the activity of bacterioplankton is stimulated by the release of dissolved organic matter (DOM) and nutrients. Since bacterioplankton groups differ in their growth requirements, such release can stimulate the growth of specific components of the bacterioplankton assemblage. Given that bacterial taxa differ in their potential for hydrolytic ectoenzyme activities and their capacity to assimilate and process various substrates (10, 22), shifts in the composition of bacterioplankton assemblages under phytoplankton blooms or oligotrophic conditions are likely to have consequences for the turnover of organic matter and biogeochemically active elements such as N and S.A component of the DOM pool that has attracted much attention for the last two decades is the algal osmolyte dimethylsulfoniopropionate (DMSP). This sulfur-containing compound is released into the water column, where it plays important roles in C and S cycling, through algal lysis or zooplankton predation. A volatile degradation product of DMSP (dimethylsulfide [DMS]) escapes to the atmosphere, where it influences climate through cloud formation (1). Bacterial utilization of DMSP is also important an...

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Acetate cycling in the water column of the Cariaco Basin: Seasonal and vertical variability and implication for carbon cycling

Cited by 83 publications

References 45 publications

Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities

Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities

Oxic water column methanogenesis as a major component of aquatic CH4 fluxes

Dimethylsulfoniopropionate Turnover Is Linked to the Composition and Dynamics of the Bacterioplankton Assemblage during a Microcosm Phytoplankton Bloom

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