Bloom of a denitrifying methanotroph, ‘<i>Candidatus</i> Methylomirabilis limnetica’, in a deep stratified lake

Graf, Jon S.; Mayr, Magdalena; Marchant, Hannah K.; Tienken, Daniela; Hach, Philipp F.; Brand, Andreas; Schubert, Carsten J.; Kuypers, Marcel M. M.; Milucka, Jana

doi:10.1111/1462-2920.14285

Cited by 88 publications

(59 citation statements)

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“…Aerobic CH 4 -oxidising microorganisms have long been recognised to play an important role in the regulation of CH 4 emissions to the atmosphere (Graf et al 2018). However, in the recent years, anaerobic oxidation of CH 4 (AOM) has been shown to be more widespread than previously predicted in areas of high organic matter availability (Evans et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Seasonal dynamics of methane cycling microbial communities in Amazonian floodplain sediments

Gontijo

Venturini

Yoshiura

et al. 2020

Preprint

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39The Amazonian floodplain forests are dynamic ecosystems of great importance for the regional 40 hydrological and biogeochemical cycles and provide a significant contribution to the global 41 carbon balance. Unique geochemical factors may drive the microbial community composition 42 and, consequently, affect CH4 emissions across floodplain areas. Here we provide the first 43 report of the in situ seasonal dynamics of CH4 cycling microbial communities in Amazonian 44 floodplains. We asked how abiotic factors may affect both overall and CH4 cycling microbial 45 communities and further investigated their responses to seasonal changes. We collected 46 sediment samples during wet and dry seasons from three different types of floodplain forests, 47 along with upland forest soil samples, from the Eastern Amazon, Brazil. We used high-48 resolution sequencing of archaeal and bacterial 16S rRNA genes combined with real-time PCR 49 to quantify Archaea and Bacteria, as well as key functional genes indicative of the 50 methanogenic (methyl coenzyme-M reductase -mcrA) and methanotrophic (particulate51 methane monooxygenase -pmoA) metabolisms. Methanogens were found to be present in 52 high abundance in floodplain sediments and they seem to resist to dramatic seasonal 53 environmental changes. Methanotrophs known to use different pathways to oxidise CH4 were 54 3 detected, including anaerobic archaeal and bacterial taxa, indicating that a wide metabolic 55 diversity may be harboured in this highly variable environment. The floodplain environmental 56 variability, which is affected by the river origin, drives not only the sediment chemistry, but also 57 the composition of the microbial communities. The results presented may contribute to the 58 understanding of the current state of CH4 cycling in this region. 59 60 Quantitative PCR. 62 63 65 et al. , 2015). These ecosystems comprise diversified and dynamic landscapes, which are 66 exposed to seasonal flooding events by the expanding rivers, as a consequence of the periodic 67 excessive rainfalls. Floodplains seem to play a significant role in the regional and global C 68 72 significant process of CH4 transfer through trees (Pangala et al., 2017). Modelling studies have 73 predicted that Amazonian floodplains may contribute up to 7% of total global CH4 emissions 74 (Potter, Melack & Engle, 2014; Wilson et al., 2016). 75In anoxic environments, the CH4 is generated as the final product of the anaerobic 76 respiration by methanogenic archaea, which can use acetate, H2/CO2, formate, CO, or 77 methylated compounds as substrates (Bridgham, Cadillo-Quiroz, Keller & Zhuang, 2013). The 78 ability to use one or more substrates varies across the different methanogenic archaea taxa. 79 Hence, substrate availability, along with other factors (biotic and abiotic), affects the diversity 80 of these organisms in the environment (Barros et al., 2019).81 103 scales. For instance, the riverine origin is a very important factor, as some waters may carry 104 large amounts of inorganic suspensoids, s...

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Section: Discussionmentioning

confidence: 99%

Seasonal dynamics of methane cycling microbial communities in Amazonian floodplain sediments

Gontijo

Venturini

Yoshiura

et al. 2020

Preprint

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“…3B and Supporting Information Fig. S3B; Text S3) may indicate obligate anaerobic methane oxidation coupled with nitrogen oxide reduction (Haroon et al, 2013;Graf et al, 2018).…”

Section: Unexpected Geomicrobiological Features In the Geochemical Prmentioning

confidence: 99%

Geomicrobiology of the carbon, nitrogen and sulphur cycles in Powell Lake: a permanently stratified water column containing ancient seawater

Haas

Desai

LaRoche

et al. 2019

Environmental Microbiology

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Summary We present the first geomicrobiological characterization of the meromictic water column of Powell Lake (British Columbia, Canada), a former fjord, which has been stably stratified since the last glacial period. Its deepest layers (300–350 m) retain isolated, relict seawater from that period. Fine‐scale vertical profiling of the water chemistry and microbial communities allowed subdivision of the water column into distinct geomicrobiological zones. These zones were further characterized by phylogenetic and functional marker genes from amplicon and shotgun metagenome sequencing. Binning of metagenomic reads allowed the linkage of function to specific taxonomic groups. Statistical analyses (analysis of similarities, Bray–Curtis similarity) confirmed that the microbial community structure followed closely the geochemical zonation. Yet, our characterization of the genetic potential relevant to carbon, nitrogen and sulphur cycling of each zone revealed unexpected features, including potential for facultative anaerobic methylotrophy, nitrogen fixation despite high ammonium concentrations and potential micro‐aerobic nitrifiers within the chemocline. At the oxic–suboxic interface, facultative anaerobic potential was found in the widespread freshwater lineage acI (Actinobacteria), suggesting intriguing ecophysiological similarities to the marine SAR11. Evolutionary divergent lineages among diverse phyla were identified in the ancient seawater zone and may indicate novel adaptations to this unusual environment.

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“…Despite growing evidence that anaerobic methanotrophs play an important role in removing methane from lake ecosystems and reducing fluxes to the atmosphere, our knowledge about the microorganisms that perform AOM, particular within lake sediments, is still rudimentary. So far, only a few studies have identified freshwater AOM‐mediating microorganisms (Ettwig et al , ; Schubert et al ; Haroon et al ; Weber et al ; Graf et al ; Versantvoort et al ). In freshwater lake sediments, methanotrophic bacteria related to Candidatus Methylomirabilis oxyfera have been reported to perform methane oxidation coupled to denitrification (Deutzmann et al ), and archaea within the phylum Euryarchaeota possibly carried out sulfate‐ and/or iron‐dependent AOM (Schubert et al ; Weber et al ).…”

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confidence: 99%

Manganese/iron‐supported sulfate‐dependent anaerobic oxidation of methane by archaea in lake sediments

Zopfi

Yao

et al. 2019

Limnology & Oceanography

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Anaerobic oxidation of methane (AOM) by methanotrophic archaea is an important sink of this greenhouse gas in marine sediments. However, evidence for AOM in freshwater habitats is rare, and little is known about the pathways, electron acceptors, and microbes involved. Here, we show that AOM occurs in anoxic sediments of a sulfate-rich lake in southern Switzerland (Lake Cadagno). Combined AOM-rate and 16S rRNA genesequencing data suggest that Candidatus Methanoperedens archaea are responsible for the observed methane oxidation. Members of the Methanoperedenaceae family were previously reported to conduct nitrate-or iron/ manganese-dependent AOM. However, we demonstrate for the first time that the methanotrophic archaea do not necessarily rely upon these oxidants as terminal electron acceptors directly, but mainly perform canonical sulfate-dependent AOM, which under sulfate-starved conditions can be supported by metal (Mn, Fe) oxides through oxidation of reduced sulfur species to sulfate. The correspondence of high abundances of Desulfobulbaceae and Candidatus Methanoperedens at the same sediment depth confirms the interdependence of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria. The relatively high abundance and widespread distribution of Candidatus Methanoperedens in lake sediments highlight their potentially important role in mitigating methane emissions from terrestrial freshwater environments to the atmosphere, analogous to ANME-1, -2, and -3 in marine settings.

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Bloom of a denitrifying methanotroph, ‘Candidatus Methylomirabilis limnetica’, in a deep stratified lake

Cited by 88 publications

References 100 publications

Seasonal dynamics of methane cycling microbial communities in Amazonian floodplain sediments

Seasonal dynamics of methane cycling microbial communities in Amazonian floodplain sediments

Geomicrobiology of the carbon, nitrogen and sulphur cycles in Powell Lake: a permanently stratified water column containing ancient seawater

Manganese/iron‐supported sulfate‐dependent anaerobic oxidation of methane by archaea in lake sediments

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