Metagenome Assembled Genome of a Novel Verrucomicrobial Methanotroph From Pantelleria Island

Picone, Nunzia; Blom, Pieter; Hogendoorn, Carmen; Frank, J. Howard; Alen, Theo van; Pol, Arjan; Gagliano, Antonina Lisa; Jetten, Mike S. M.; D’Alessandro, Walter; Quatrini, Paola; Camp, Huub J. M. Op den

doi:10.3389/fmicb.2021.666929

Cited by 14 publications

(23 citation statements)

References 61 publications

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“…Acidophilic verrucomicrobial methanotrophs have been shown to encode the complete H4F pathway (Picone et al 2021 , Schmitz et al 2021 ), but none in this study did, only a partial one if at all. Thus, the formaldehyde oxidation step remains unclear in the Verrucomicrobiota analyzed herein.…”

Section: Discussionmentioning

confidence: 52%

Metagenomics and metatranscriptomics reveal broadly distributed, active, novel methanotrophs in the Gulf of Mexico hypoxic zone and in the marine water column

Howe

Seitz²,

Campbell

et al. 2022

FEMS Microbiology Ecology

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The northern Gulf of Mexico (nGOM) hypoxic zone is a shallow water environment where methane, a potent greenhouse gas, fluxes from sediments to bottom water and remains trapped due to summertime stratification. When the water column is destratified, an active planktonic methanotrophic community could mitigate the efflux of methane, which accumulates to high concentrations, to the atmosphere. To investigate the possibility of such a biofilter in the nGOM hypoxic zone we performed metagenome assembly, and metagenomic and metatranscriptomic read mapping. Methane monooxygenase (pmoA) was an abundant transcript, yet few canonical methanotrophs have been reported in this environment, suggesting a role for non-canonical methanotrophs. To determine the identity of these methanotrophs, we reconstructed six novel metagenome-assembled genomes (MAGs), in the Planctomycetota, Verrucomicrobiota, and one putative Latescibacterota, each with at least one pmoA gene copy. Based on ribosomal protein phylogeny, closely related microbes (mostly from Tara Oceans) and isolate genomes were selected and co-analyzed with the nGOM MAGs. Gene annotation and read mapping suggested that there is a large, diverse, and unrecognized community of active aerobic methanotrophs in the nGOM hypoxic zone and in the global ocean that could mitigate methane flux to the atmosphere.

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Section: Discussionmentioning

confidence: 52%

Metagenomics and metatranscriptomics reveal broadly distributed, active, novel methanotrophs in the Gulf of Mexico hypoxic zone and in the marine water column

Howe

Seitz²,

Campbell

et al. 2022

FEMS Microbiology Ecology

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show abstract

“…To overcome these limitations, prokaryotic systematists have embraced and integrated whole genome sequence-based analyses in their practices [ 3 , [15] , [16] , [17] , [18] , [19] , [20] ]. Not only it resolved the taxonomic status of complex taxon [ [17] , [18] , [19] , 21 , 22 ], but it is also now possible to define new species of unculturable prokaryotes based on single-amplified genomes and metagenome-assembled genomes [ [23] , [24] , [25] ].…”

Section: Introductionmentioning

confidence: 99%

Advanced prokaryotic systematics: the modern face of an ancient science

Nouioui¹,

Sangal²

2022

New Microbes and New Infections

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“…A third organism, Ca. Methylacidithermus pantelleriae, from a metagenome-assembled genome (MAG) represents the only known member of this proposed genus (Picone et al, 2021b). All three genera are characterized by being the only bacteria capable of oxidizing methane (methanotrophy) in extremely acidic environments (van Teeseling et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Phylogenetic profiles of Verrucomicrobia acidophiles have been based on analyses using 16S rRNA (Dunfield et al, 2007;Pol et al, 2007;van Teeseling et al, 2014;Picone et al, 2021b;Schmitz et al, 2021), pmoA (Anvar et al, 2014;Picone et al, 2021a), or seven housekeeping genes (Erikstad et al, 2019). In this paper, we extend the phylogenetic analyses of this group using fully sequenced genomic data, including all sequenced genomes of Verrucomicrobia methanotrophs.…”

Section: Introductionmentioning

confidence: 99%

Genome-guided prediction of acid resistance mechanisms in acidophilic methanotrophs of phylogenetically deep-rooted Verrucomicrobia isolated from geothermal environments

2022

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Verrucomicrobia are a group of microorganisms that have been proposed to be deeply rooted in the Tree of Life. Some are methanotrophs that oxidize the potent greenhouse gas methane and are thus important in decreasing atmospheric concentrations of the gas, potentially ameliorating climate change. They are widespread in various environments including soil and fresh or marine waters. Recently, a clade of extremely acidophilic Verrucomicrobia, flourishing at pH < 3, were described from high-temperature geothermal ecosystems. This novel group could be of interest for studies about the emergence of life on Earth and to astrobiologists as homologs for possible extraterrestrial life. In this paper, we describe predicted mechanisms for survival of this clade at low pH and suggest its possible evolutionary trajectory from an inferred neutrophilic ancestor. Extreme acidophiles are defined as organisms that thrive in extremely low pH environments (≤ pH 3). Many are polyextremophiles facing high temperatures and high salt as well as low pH. They are important to study for both providing fundamental insights into biological mechanisms of survival and evolution in such extreme environments and for understanding their roles in biotechnological applications such as industrial mineral recovery (bioleaching) and mitigation of acid mine drainage. They are also, potentially, a rich source of novel genes and pathways for the genetic engineering of microbial strains. Acidophiles of the Verrucomicrobia phylum are unique as they are the only known aerobic methanotrophs that can grow optimally under acidic (pH 2–3) and moderately thermophilic conditions (50–60°C). Three moderately thermophilic genera, namely Methylacidiphilum, Methylacidimicrobium, and Ca. Methylacidithermus, have been described in geothermal environments. Most of the investigations of these organisms have focused on their methane oxidizing capabilities (methanotrophy) and use of lanthanides as a protein cofactor, with no extensive study that sheds light on the mechanisms that they use to flourish at extremely low pH. In this paper, we extend the phylogenetic description of this group of acidophiles using whole genome information and we identify several mechanisms, potentially involved in acid resistance, including “first line of defense” mechanisms that impede the entry of protons into the cell. These include the presence of membrane-associated hopanoids, multiple copies of the outer membrane protein (Slp), and inner membrane potassium channels (kup, kdp) that generate a reversed membrane potential repelling the intrusion of protons. Acidophilic Verrucomicrobia also display a wide array of proteins potentially involved in the “second line of defense” where protons that evaded the first line of defense and entered the cell are expelled or neutralized, such as the glutamate decarboxylation (gadAB) and phosphate-uptake systems. An exclusive N-type ATPase F0-F1 was identified only in acidophiles of Verrucomicrobia and is predicted to be a specific adaptation in these organisms. Phylogenetic analyses suggest that many predicted mechanisms are evolutionarily conserved and most likely entered the acidophilic lineage of Verrucomicrobia by vertical descent from a common ancestor. However, it is likely that some defense mechanisms such as gadA and kup entered the acidophilic Verrucomicrobia lineage by horizontal gene transfer.

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Metagenome Assembled Genome of a Novel Verrucomicrobial Methanotroph From Pantelleria Island

Cited by 14 publications

References 61 publications

Metagenomics and metatranscriptomics reveal broadly distributed, active, novel methanotrophs in the Gulf of Mexico hypoxic zone and in the marine water column

Metagenomics and metatranscriptomics reveal broadly distributed, active, novel methanotrophs in the Gulf of Mexico hypoxic zone and in the marine water column

Advanced prokaryotic systematics: the modern face of an ancient science

Genome-guided prediction of acid resistance mechanisms in acidophilic methanotrophs of phylogenetically deep-rooted Verrucomicrobia isolated from geothermal environments

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