Marine methane paradox explained by bacterial degradation of dissolved organic matter

Repeta, Daniel J.; Ferrón, Sara; Sosa, Oscar A.; Johnson, C. G.; Repeta, Lucas; Acker, Marianne; DeLong, Edward F.; Karl, David M.

doi:10.1038/ngeo2837

Cited by 269 publications

(334 citation statements)

References 42 publications

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“…Since the seawater was not pre-filtered through a larger pore-size filter, which would exclude larger particles but allow bacterial cells to pass, production of methane in microanoxic zones (de Angelis and Lee, 1994;Oremland, 1979) should be considered. Furthermore, several studies suggested pathways for methane production in oxygenated marine systems from methylated compounds or dissolved organic matter (Damm et al, 2010;Florez-Leiva et al, 2010;Karl et al, 2008;Repeta et al, 2016). The methane production rate of 0.06 nmol L −1 d −1 observed in our study is 2 to 6 orders of magnitude lower than previously published methane production rates under aerobic conditions (Damm et al, 2010;Karl et al, 2008).…”

Section: Methane Dynamics At Different Methane Concentrationscontrasting

confidence: 53%

“…In the ocean, the two major sources of methane are ongoing biogenic production by microbes in anoxic sediment (Formolo, 2010;Reeburgh, 2007;Whiticar, 1999) and release of fossil methane from geological storage (summarized by Kvenvolden and Rogers, 2005;Saunois et al, 2016). Other sources include release from permafrost, river runoff, submarine groundwater discharge (Lecher et al, 2016;Overduin et al, 2012), and production from methylated substrates under aerobic conditions (Damm et al, 2010;Karl et al, 2008;Repeta et al, 2016). More than 90 % of the methane sourced in the seabed is oxidized within the sediment by anaerobic and aerobic oxidation (Barnes and Goldberg, 1976;Boetius and Wenzhöfer, 2013;Knittel and Boetius, 2009;Reeburgh, 1976).…”

Section: Introductionmentioning

confidence: 99%

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Methane-oxidizing seawater microbial communities from an Arctic shelf

et al. 2018

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Abstract. Marine microbial communities can consume dissolved methane before it can escape to the atmosphere and contribute to global warming. Seawater over the shallow Arctic shelf is characterized by excess methane compared to atmospheric equilibrium. This methane originates in sediment, permafrost, and hydrate. Particularly high concentrations are found beneath sea ice. We studied the structure and methane oxidation potential of the microbial communities from seawater collected close to Utqiagvik, Alaska, in April 2016. The in situ methane concentrations were 16.3 ± 7.2 nmol L −1 , approximately 4.8 times oversaturated relative to atmospheric equilibrium. The group of methaneoxidizing bacteria (MOB) in the natural seawater and incubated seawater was > 97 % dominated by Methylococcales (γ -Proteobacteria). Incubations of seawater under a range of methane concentrations led to loss of diversity in the bacterial community. The abundance of MOB was low with maximal fractions of 2.5 % at 200 times elevated methane concentration, while sequence reads of non-MOB methylotrophs were 4 times more abundant than MOB in most incubations. The abundances of MOB as well as non-MOB methylotroph sequences correlated tightly with the rate constant (k ox ) for methane oxidation, indicating that non-MOB methylotrophs might be coupled to MOB and involved in community methane oxidation. In sea ice, where methane concentrations of 82 ± 35.8 nmol kg −1 were found, Methylobacterium (α-Proteobacteria) was the dominant MOB with a relative abundance of 80 %. Total MOB abundances were very low in sea ice, with maximal fractions found at the icesnow interface (0.1 %), while non-MOB methylotrophs were present in abundances similar to natural seawater communities. The dissimilarities in MOB taxa, methane concentrations, and stable isotope ratios between the sea ice and water column point toward different methane dynamics in the two environments.

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Section: Methane Dynamics At Different Methane Concentrationscontrasting

confidence: 53%

Section: Introductionmentioning

confidence: 99%

Methane-oxidizing seawater microbial communities from an Arctic shelf

et al. 2018

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“…Targeted metabolomic studies focus on individual, well-characterized substrates whose concentrations and cycling can be followed precisely in incubations and in field settings. Advantages of such an approach are clear -in general, targeted work is quantitative, precise, and the metabolic role of identified substrates may already be well established (Amin et al, 2015;Johnson et al, 2016;Repeta et al, 2016;Heal et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…These molecules have been identified in culture experiments and/or detected in field samples to highlight some of the important microbial interactions in the surface ocean (Amin et al, 2015;Johnson et al, 2016;Repeta et al, 2016;Heal et al, 2017;Kujawinski et al, 2017). Targeted metabolomic studies focus on individual, well-characterized substrates whose concentrations and cycling can be followed precisely in incubations and in field settings.…”

Section: Introductionmentioning

confidence: 99%

High-Resolution Liquid Chromatography Tandem Mass Spectrometry Enables Large Scale Molecular Characterization of Dissolved Organic Matter

et al. 2017

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Dissolved organic matter (DOM) is arguably one of the most complex exometabolomes on earth, and is comprised of thousands of compounds, that together contribute more than 600 × 10 15 g carbon. This reservoir is primarily the product of interactions between the upper ocean's microbial food web, yet abiotic processes that occur over millennia have also modified many of its molecules. The compounds within this reservoir play important roles in determining the rate and extent of element exchange between inorganic reservoirs and the marine biosphere, while also mediating microbe-microbe interactions. As such, there has been a widespread effort to characterize DOM using high-resolution analytical methods including nuclear magnetic resonance spectroscopy (NMR) and mass spectrometry (MS). To date, molecular information in DOM has been primarily obtained through calculated molecular formulas from exact mass. This approach has the advantage of being non-targeted, accessing the inherent complexity of DOM. Molecular structures are however still elusive and the most commonly used instruments are costly. More recently, tandem mass spectrometry has been employed to more precisely identify DOM components through comparison to library mass spectra. Here we describe a data acquisition and analysis workflow that expands the repertoire of high-resolution analytical approaches available to access the complexity of DOM molecules that are amenable to electrospray ionization (ESI) MS. We couple liquid chromatographic separation with tandem MS (LC-MS/MS) and a data analysis pipeline, that integrates peak extraction from extracted ion chromatograms (XIC), molecular formula calculation and molecular networking. This provides more precise structural characterization. Although only around 1% of detectable DOM compounds can be annotated through publicly available spectral libraries, community-wide participation in populating and annotating DOM datasets could rapidly increase the annotation rate and should be broadly encouraged. Our analysis also identifies shortcomings of the current Petras et al. LC-MS/MS Analysis of DOMdata analysis workflow that need to be addressed by the community in the future. This work will lay the foundation for an integrative, non-targeted molecular analysis of DOM which, together with next generation sequencing, meta-proteomics and physical data, will pave the way to a more comprehensive understanding of the role of DOM in structuring marine ecosystems.

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“…The production and hydrolysis of reduced compounds like phosphonates are of particular interest because the hydrolysis of methylphosphonate has the potential to release methane, a potent greenhouse gas (Karl et al, 2008;Repeta et al, 2016 likely performs the irreversible conversion of phosphonopyruvate to phosphonoacetaldehyde which prevents reversion to the ester bond structure. Finally, the presence of the gene for 2-aminoethylphosphonic acid pyruvate-transaminase (2-AEP-TA) suggests that phosphonoacetaldehyde is further converted to 2-aminoethylphosphonate (2-AEP), the organophosphonate that occurs most commonly in the environment (McGrath et al, 2013).…”

Section: Phosphonate Biosynthesis By Trichodesmium In the Wtspmentioning

confidence: 99%

<i>Trichodesmium</i> physiological ecology and phosphate reduction in the western Tropical South Pacific

Frischkorn¹,

Krupke²,

Rouco³

et al. 2018

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Marine methane paradox explained by bacterial degradation of dissolved organic matter

Cited by 269 publications

References 42 publications

Methane-oxidizing seawater microbial communities from an Arctic shelf

Methane-oxidizing seawater microbial communities from an Arctic shelf

High-Resolution Liquid Chromatography Tandem Mass Spectrometry Enables Large Scale Molecular Characterization of Dissolved Organic Matter

<i>Trichodesmium</i> physiological ecology and phosphate reduction in the western Tropical South Pacific

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Marine methane paradox explained by bacterial degradation of dissolved organic matter

Cited by 269 publications

References 42 publications

Methane-oxidizing seawater microbial communities from an Arctic shelf

Methane-oxidizing seawater microbial communities from an Arctic shelf

High-Resolution Liquid Chromatography Tandem Mass Spectrometry Enables Large Scale Molecular Characterization of Dissolved Organic Matter

&lt;i&gt;Trichodesmium&lt;/i&gt; physiological ecology and phosphate reduction in the western Tropical South Pacific

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<i>Trichodesmium</i> physiological ecology and phosphate reduction in the western Tropical South Pacific