Anaerobic oxidation of methane and associated microbiome in anoxic water of Northwestern Siberian lakes

Cabrol, Léa; Thalasso, Frédéric; Gandois, Laure; Sepulveda‐Jauregui, Armando; Martinez‐Cruz, Karla; Teisserenc, Roman; Tananaev, Nikita; Tveit, Alexander Tøsdal; Svenning, Mette M.; Barret, Maialen

doi:10.1016/j.scitotenv.2020.139588

“…MOB throughout the water column of Rotsee play a prominent role in mitigating CH 4 emissions to the atmosphere (Schubert et al, 2010;Oswald et al, 2015). The dominance of type I MOB (Methylobacter, Methylomonas, Methylosoma, type Ia, and type Ib) over type II MOB (Methylocystis) is consistent with previously reported patterns in Rotsee and other freshwater lakes (Borrel et al, 2011;Bornemann et al, 2016;Oswald et al, 2016b;Rissanen et al, 2018;Mayr et al, 2019;Cabrol et al, 2020;Reis et al, 2020). Evidence for the presence of anaerobic MOB in Rotsee, such as NC10 (Methylomirabilis sp.…”

Section: Discussionsupporting

confidence: 84%

“…However, it is possible that these MOB rely on Fe for other enzymatic pathways (e.g., formate dehydrogenase; Glass and Orphan, 2012). Furthermore, it has been suggested that the mechanism of Fe-coupled anaerobic CH 4 oxidation is accomplished by a complex microbe-mineral reaction network in which both, MOB and iron-reducing organisms (bacteria and archaea) are directly and indirectly involved (Bar-Or et al, 2017;Cabrol et al, 2020). For example, besides methanogens being able to produce CH 4 , they are additionally involved in reducing Fe-oxides at high CH 4 concentrations leading to intermediates, which are required by MOB for CH 4 oxidation (Bar-Or et al, 2017).…”

Section: Metals Are Important Drivers Of Mob Community Compositionmentioning

confidence: 99%

Environmental and Microbial Interactions Shape Methane-Oxidizing Bacterial Communities in a Stratified Lake

Guggenheim

¹

,

Freimann

²

,

Mayr

³

et al. 2020

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In stratified lakes, methane-oxidizing bacteria (MOB) are strongly mitigating methane fluxes to the atmosphere by consuming methane entering the water column from the sediments. MOB communities in lakes are diverse and vertically structured, but their spatio-temporal dynamics along the water column as well as physico-chemical parameters and interactions with other bacterial species that drive the community assembly have so far not been explored in depth. Here, we present a detailed investigation of the MOB and bacterial community composition and a large set of physico-chemical parameters in a shallow, seasonally stratified, and sub-alpine lake. Four highly resolved vertical profiles were sampled in three different years and during various stages of development of the stratified water column. Non-randomly assembled MOB communities were detected in all compartments. We could identify methane and oxygen gradients and physico-chemical parameters like pH, light, available copper and iron, and total dissolved nitrogen as important drivers of the MOB community structure. In addition, MOB were well-integrated into a bacterial-environmental network. Partial redundancy analysis of the relevance network of physico-chemical variables and bacteria explained up to 84% of the MOB abundances. Spatio-temporal MOB community changes were 51% congruent with shifts in the total bacterial community and 22% of variance in MOB abundances could be explained exclusively by the bacterial community composition. Our results show that microbial interactions may play an important role in structuring the MOB community along the depth gradient of stratified lakes.

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“…Pure cultures of the gammaproteobacterial and alphaproteobacterial methanotrophs Methylomonas and Methylosinus coupled methane oxidation to ferrihydrite reduction under the availability of 0.89 mg O 2 L −1 (Zheng et al, 2020). Bacterial methanotrophs were suggested to account for Fe‐AOM in oxygen‐depleted incubations with sediments from Lake Kinneret in Israel (Bar‐Or et al, 2017) and in anoxic waters of Northwestern Siberian lakes (Cabrol et al, 2020). How methane may be activated by PMO in the absence of oxygen or at nanomolar concentrations of oxygen is not yet known, but could have similarities to the mechanism employed by Ca .…”

Section: Introductionmentioning

confidence: 99%

Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments

Martins

¹

,

A

²

,

Lenstra

³

et al. 2021

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Microbial methane oxidation is a major biofilter preventing larger emissions of this powerful greenhouse gas from marine coastal areas into the atmosphere. In these zones, various electron acceptors such as sulfate, metal oxides, nitrate, or oxygen can be used. However, the key microbial players and mechanisms of methane oxidation are poorly understood. In this study, we inoculated a bioreactor with methane‐ and iron‐rich sediments from the Bothnian Sea to investigate microbial methane and iron cycling under low oxygen concentrations. Using metagenomics, we investigated shifts in microbial community composition after approximately 2.5 years of bioreactor operation. Marker genes for methane and iron cycling, as well as respiratory and fermentative metabolism, were identified and used to infer putative microbial metabolism. Metagenome‐assembled genomes representing novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria were recovered and revealed a potential for methane oxidation, organic matter degradation, and iron cycling, respectively. This work brings new hypotheses on the identity and metabolic versatility of microorganisms that may be members of such functional guilds in coastal marine sediments and highlights that microorganisms potentially composing the methane biofilter in these sediments may be more diverse than previously appreciated.

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“…In that study, pmoA copy numbers followed trends of δ 13 CDIC and iron (II) indicative of Fe-AOM. More recently, Methylomonadaceae were suggested to account for methane oxidation in anoxic waters of Northwestern Siberian lakes (18). The authors hypothesized that iron (III) could be the electron acceptor for AOM because of total iron concentrations and the identification of taxa known to perform iron reduction.…”

Section: Enrichment Of a Novel Verrucomicrobia Bacteroidetes And Krmentioning

confidence: 99%

“…Pure cultures of the gammaproteobacterial and alphaproteobacterial methanotrophs Methylomonas and Methylosinus were shown to couple methane oxidation to ferrihydrite reduction under the availability of 0.89 mg O2 L -1 (16). Bacterial methanotrophs were suggested to account for Fe-AOM in oxygen-depleted incubations with sediments from Lake Kinneret in Israel (17) and in anoxic waters of Northwestern Siberian lakes (18). How methane may be activated by PMO in the absence of oxygen or at nanomolar concentrations of oxygen is not yet known, but could have similarities to the mechanism employed by Ca.…”

Section: Introductionmentioning

confidence: 99%

Enrichment of novelVerrucomicrobia, BacteroidetesandKrumholzibacteriain an oxygen-limited, methane- and iron-fed bioreactor inoculated with Bothnian Sea sediments

Martins

¹

,

A

²

,

Lenstra

³

et al. 2020

Preprint

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Microbial methane oxidation is a major biofilter preventing larger emissions of this powerful greenhouse gas from marine coastal areas into the atmosphere. In these zones, various electron acceptors such as sulfate, metal oxides, nitrate or oxygen can be utilized. However, the key microbial players and mechanisms of methane oxidation are poorly understood. In this study, we inoculated a bioreactor with methane- and iron-rich sediments from the Bothnian Sea in order to investigate microbial methane and iron cycling under low oxygen concentrations. Using metagenomics, we observed shifts in the microbial community over approximately 2.5 years of bioreactor operation. Marker genes for methane and iron cycling, as well as respiratory and fermentative metabolism, were investigated. Metagenome-assembled genomes representing novel Verrucomicrobia, Bacteroidetes and Krumholzibacteria were recovered and revealed potential for methane oxidation, organic matter degradation, and iron cycling, respectively. This work brings new insights into the identity and metabolic versatility of microorganisms that may be members of such functional guilds in coastal marine sediments and highlights that the methane biofilter in these sediments may be more diverse than previously appreciated. Importance: Despite the essential role of microorganisms in preventing most methane in the ocean floor to reach the atmosphere, comprehensive knowledge on the identity and the mechanisms employed by these microorganisms is still lacking. This is problematic because such information is needed to understand how the ecosystem functions in the present and how microorganisms may respond to climate change in the future. Here, we enriched and identified novel taxa potentially involved in methane and iron cycling in an oxygen-limited bioreactor inoculated with methane- and iron-rich coastal sediments. Metagenomic analyses provided hypotheses about the mechanisms they may employ, such as the use of oxygen at very low concentrations. The implication of our results is that in more shallow sediments, where oxygen-limited conditions are present, the methane biofilter is potentially composed of novel, metabolically versatile Verrucomicrobia that could contribute to mitigating methane emissions from coastal marine zones.

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Anaerobic oxidation of methane and associated microbiome in anoxic water of Northwestern Siberian lakes

Cited by 74 publications

References 105 publications

Environmental and Microbial Interactions Shape Methane-Oxidizing Bacterial Communities in a Stratified Lake

Environmental and Microbial Interactions Shape Methane-Oxidizing Bacterial Communities in a Stratified Lake

Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments

Enrichment of novelVerrucomicrobia, BacteroidetesandKrumholzibacteriain an oxygen-limited, methane- and iron-fed bioreactor inoculated with Bothnian Sea sediments

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