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

Su, Guangyi; Zopfi, Jakob; Yao, Haoyi; Steinle, Lea; Niemann, Helge; Lehmann, Moritz F.

doi:10.1002/lno.11354

Cited by 67 publications

(74 citation statements)

References 80 publications

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“…In the floodplain sediments, we detected both archaeal and bacterial taxa with the reported capability to carry out anaerobic CH 4 oxidation. For instance, the methanogenic family Methanoperedenaceae (Timmers et al 2017) has been proposed as a potential anaerobic methanotrophic archaeal (ANME) group, using the nitrate-dependent reverse methanogenesis (Yan & Ferry, 2018) or in consortia with sulphate-reducing bacteria (Su et al, 2019). Here we found a positive correlation between Metanoperedenaceae relative abundance and Mn contents of the sediment.…”

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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“…Marine ANME lineages are often observed to form consortia with SRB, with ANME-1 and ANME-2 (a, b, and c) being associated with multiple genera within the Desulfobacterales and Desulfobulbaceae (13,(16)(17)(18)(19)(20), thermophilic ANME-1 being associated with "Candidatus Desulfofervidus auxilii" (8,21), and ANME-3 being associated with SRBs of the Desulfobulbus (22). While members of the family Methanoperedenaceae have also recently been associated with SRB of the family Desulfobulbaceae in a freshwater lake sediment (23), they also appear to oxidize methane independently using a range of electron acceptors. The type species of this family, "Candidatus Methanoperedens nitroreducens," was originally enriched in a bioreactor and shown to couple AOM to the reduction of nitrate via a laterally transferred nitrate reductase (15).…”

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confidence: 99%

Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae

Leu

McIlroy

et al. 2020

mBio

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Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceae metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate and the reduction of arsenate, selenate, and elemental sulfur. Numerous membrane-bound multiheme c-type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humic substances, and syntrophic partners. IMPORTANCE AOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance for the global carbon cycle and climate change modeling. While the oxidation of methane coupled to sulfate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study, we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae, as they are absent from related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles.

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“…Willersinnweiher. However, it is more likely that Mn supports sedimentary anaerobic CH 4 oxidation via SO 4 2− through reoxidation of reduced S species, as it was also recently described for Lake Cadagno (Su et al 2019).…”

Section: Discussionmentioning

confidence: 53%

The impact of seasonal sulfate–methane transition zones on methane cycling in a sulfate‐enriched freshwater environment

Kleint

Wellach

Schroll

et al. 2021

Limnology & Oceanography

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Lake Willersinnweiher located in south-western Germany is a small eutrophic gravel pit lake fed by sulfateenriched groundwater. The aim of this study was to investigate the total methane (CH 4 ) mass balance of Lake Willersinnweiher with a particular focus on the interaction of carbon and sulfur cycling within the lake sediments and the redoxcline of the water column. Our results show that Lake Willersinnweiher permanently releases CH 4 to the atmosphere throughout the whole year 2018 at rates ranging from 5 to 120 mol d −1 . Sediment data show the presence of intense anaerobic oxidation of CH 4 in the upper sediment layers during early summer. Here, CH 4 is most likely consumed via sulfate in sulfate-methane transition zones (SMTZs) that have been observed for a few specific freshwater environments only. Seasonal dynamics in biogeochemical processes trigger the non-steady state conditions within the sediments and the CH 4 consumption in the SMTZs. In parallel, CH 4 released from the sediments is completely consumed by aerobic oxidation processes in the redoxcline indicated by minimum CH 4 concentrations with high δ 13 C-CH 4 values. This zone acts as an effective barrier, minimizing CH 4 release into the surface water and the atmosphere and thus CH 4 oversaturation along with near-atmospheric isotopic composition indicate the presence of an additional CH 4 source in the epilimnion of Lake Willersinnweiher.The emission of the greenhouse gas methane (CH 4 ) from freshwater lakes has been suggested to play a substantial role in the global methane budget (e.g., Bastviken et al. 2004). Here, significant amounts of CH 4 are emitted, even though CH 4 produced in aquatic systems is largely consumed by anaerobic and aerobic methanotrophs (up to 30-99%; Bastviken et al. 2008). The amount of emitted CH 4 is thereby depending on bioproduction, degradation and mineralization of organic substances in the sediments and the water column of the freshwater lake.Carbon mineralization in anoxic lake sediments is affected by manganese (Mn) and iron (Fe) reducing bacteria metabolizing competitive substrates, outcompeting CH 4 forming microorganisms (methanogens) within the upper sediment layers (e.g., Whiticar 1999). Sulfate (SO 4 2− ) reduction often has minor implications on organic matter degradation due to low SO 4 2− availability in most freshwater environments (Holmer and Storkholm 2001), so that SO 4 2− is rapidly depleted with sediment depth and SO 4 2− reducing bacteria become inactive or are absent. As a consequence, methanogenesis is the most important process in overall carbon mineralization in anoxic lacustrine sediments (e.g., Rudd and Hamilton 1978). Competitive metabolisms are not only affecting methanogenesis, but also consumption of CH 4 by bacteria (methanotrophs) in the sediments. The anaerobic oxidation of methane in the sediments of lakes is usually coupled to the reduction of the energetically more favorable electron acceptors, such as nitrate and nitrite (e.g., Raghoebarsing et al. 2006) or Fe(III) and/or Mn(I...

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

Cited by 67 publications

References 80 publications

Seasonal dynamics of methane cycling microbial communities in Amazonian floodplain sediments

Seasonal dynamics of methane cycling microbial communities in Amazonian floodplain sediments

Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family Methanoperedenaceae

The impact of seasonal sulfate–methane transition zones on methane cycling in a sulfate‐enriched freshwater environment

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