Enrichment of anaerobic nitrate-dependent methanotrophic ‘Candidatus Methanoperedens nitroreducens’ archaea from an Italian paddy field soil

Vaksmaa, Annika; Guerrero-Cruz, Simon; Alen, Theo A. van; Cremers, Geert; Ettwig, Katharina F.; Lüke, Claudia; Jetten, Mike S. M.

doi:10.1007/s00253-017-8416-0

Cited by 116 publications

(101 citation statements)

References 31 publications

(31 reference statements)

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“…As previously reported, the MAGs M.Nitro, BLZ2, and IPS-1 encode respiratory nitrate reductases that are part of the CISM superfamily, allowing them to independently mediate AOM coupled to nitrate reduction (15, 24, 65). Based on phylogenetic analysis ( Figure 3 ), genes encoding cytoplasmic nitrite oxidoreductases (NxrA) were identified in the IPS-1, BLZ2, and M.Nitro MAGs, and a nitrate reductase closely related to NarG proteins was identified in the BLZ2 MAG.…”

Section: Resultsmentioning

confidence: 68%

Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal familyMethanoperedenaceae

McIlroy

Leu

et al. 2020

Preprint

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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 Methanoperedenaceace 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 multi-heme c type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humics and syntrophic partners.ImportanceAOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance to the global carbon cycle and climate change modelling. While the oxidation of methane coupled to sulphate 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 in 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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Section: Resultsmentioning

confidence: 68%

Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal familyMethanoperedenaceae

McIlroy

Leu

et al. 2020

Preprint

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“…strain BLZ2. Analysis of the microbial community in the Italian paddy field ANME-2d enrichment has been described by Vaksmaa et al, 2017. For this bioreactor a similar proportion (22%) of ANME-2d archaea, in this case Ca .…”

Section: Resultsmentioning

confidence: 98%

“…Under these conditions nitrite was not detectable with a colorimetric test with a lower detection limit of 2 mg/L (MQuant test stripes, Merck, Darmstadt, Germany). Growth conditions and operation of the bioreactor containing ANME-2d archaea enriched from an Italian paddy field soil are described by Vaksmaa et al ., 2017 (Vaksmaa, Jetten, et al , 2017). Sampled material from both reactors was centrifuged (10000 x g , 20 min, 4°C) and pellets were kept at −80°C until subsequent freeze-drying and following lipid and isotope analysis.…”

Section: Methodsmentioning

confidence: 99%

“…Instead, ANME-2d archaea are the main players in nitrate-dependent AOM. Microorganisms conducting nitrate AOM have been enriched from anoxic freshwater sediments, digester sludge and rice paddies (Raghoebarsing et al , 2006; Hu et al , 2009; Arshad et al , 2015; Vaksmaa, Guerrero-Cruz, et al , 2017). Denitrifying AOM can either be conducted by a consortium of nitrate-reducing ANMEs, Ca .…”

Section: Introductionmentioning

confidence: 99%

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ANME-2d anaerobic methanotrophic archaea differ from other ANME archaea in lipid composition and carbon source

Kurth

Smit

Berger

et al. 2019

Preprint

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The anaerobic oxidation of methane (AOM) is a microbial process present in marine and freshwater environments. AOM is important for reducing the emission of the second most important greenhouse gas methane. In marine environments anaerobic methanotrophic archaea (ANME) are involved in sulfate-reducing AOM. In contrast, Ca. Methanoperedens of the ANME-2d cluster carries out nitrate AOM in freshwater ecosystems. Despite the importance of those organisms for AOM in non-marine environments not much is known about their lipid composition or carbon sources. To close this gap, we analyzed the lipid composition of ANME-2d archaea and found that they mainly synthesize archaeol and hydroxyarchaeol as well as different (hydroxy-) glycerol dialkyl glycerol tetraethers, albeit in much lower amounts. Abundant lipid headgroups were dihexose, monomethyl-phosphatidyl ethanolamine and phosphatidyl hexose. Moreover, a monopentose was detected as a lipid headgroup which is rare among microorganisms. Batch incubations with 13C labelled bicarbonate and methane showed that methane is the main carbon source of ANME-2d archaea varying from ANME-1 archaea which primarily assimilate dissolved inorganic carbon (DIC). ANME-2d archaea also assimilate DIC, but to a lower extent than methane. The lipid characterization and analysis of the carbon source of Ca. Methanoperedens facilitates distinction between ANME-2d and other ANMEs.

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“…When nitrate and nitrite were supplied together to anoxic sediments collected from agricultural ditch canals, both nitrate-and nitrite-dependent methane-oxidizing microorganisms were enriched (6,36). Enrichments solely fed with nitrate resulted in similar cocultures where nitrate-AOM supports nitrite-AOM by producing nitrite (10,37,38). On the other hand, when ammonium, methane, and nitrite were supplied as substrates, cocultures of Methylomirabilis species and anaerobic ammonium-oxidizing (anammox) bacteria were achieved (14,(39)(40)(41).…”

mentioning

confidence: 99%

Key Physiology of a Nitrite-Dependent Methane-Oxidizing Enrichment Culture

Guerrero-Cruz

Stultiens

Kessel

et al. 2019

Appl Environ Microbiol

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Nitrite-dependent methane-oxidizing bacteria couple the reduction of nitrite to the oxidation of methane via a unique oxygen-producing pathway. This process is carried out by members of the genus Methylomirabilis that belong to the NC10 phylum. Contrary to other known anaerobic methane oxidizers, they do not employ the reverse methanogenesis pathway for methane activation but instead a canonical particulate methane monooxygenase similar to those used by aerobic methanotrophs. Methylomirabilis-like bacteria are detected in many natural and manmade ecosystems, but their physiology is not well understood. Here, using continuous cultivation techniques, batch activity assays, and state-of-the-art membrane-inlet mass spectrometry, we determined growth rate, doubling time, and methane and nitrite affinities of the nitrite-dependent methane-oxidizing bacterium "Candidatus Methylomirabilis lanthanidiphila." Our results provide insight into understanding the interactions of these microorganisms with methanotrophs and other nitrite-reducing microorganisms, such as anaerobic ammonium-oxidizing bacteria. Furthermore, our data can be used in modeling studies as well as wastewater treatment plant design. IMPORTANCE Methane is an important greenhouse gas with a radiative forcing 28 times that of carbon dioxide over a 100-year time scale. The emission of methane to the atmosphere is controlled by aerobic and anaerobic methanotrophs, which are microorganisms that are able to oxidize methane to conserve energy. While aerobic methanotrophs have been studied for over a century, knowledge on the physiological characteristics of anaerobic methanotrophs is scarce. Here, we describe kinetic properties of "Candidatus Methylomirabilis lanthanidiphila," a nitrite-dependent methane-oxidizing microorganism, which is ecologically important and can be applied in wastewater treatment.

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Enrichment of anaerobic nitrate-dependent methanotrophic ‘Candidatus Methanoperedens nitroreducens’ archaea from an Italian paddy field soil

Cited by 116 publications

References 31 publications

Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal familyMethanoperedenaceae

Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal familyMethanoperedenaceae

ANME-2d anaerobic methanotrophic archaea differ from other ANME archaea in lipid composition and carbon source

Key Physiology of a Nitrite-Dependent Methane-Oxidizing Enrichment Culture

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