PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference

Keltjens, Jan T.; Pol, Arjan; Reimann, Joachim; Camp, Huub J. M. Op den

doi:10.1007/s00253-014-5766-8

Cited by 333 publications

(468 citation statements)

References 135 publications

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“…Previous work showed that the lanthanide-dependent XoxF-type MDH enzymes are more widespread than the classical MxaFtype MDH enzymes in known methylotrophs and other organisms (40)(41)(42). In line with previous findings with other methanotrophs (26,27), we provide evidence that in pure culture in the presence of lanthanum the XoxF-type (Fig.…”

Section: Discussionsupporting

confidence: 81%

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Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions

Krause

Johnson

Karunaratne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

161

144

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The utilization of methane, a potent greenhouse gas, is an important component of local and global carbon cycles that is characterized by tight linkages between methane-utilizing (methanotrophic) and nonmethanotrophic bacteria. It has been suggested that the methanotroph sustains these nonmethanotrophs by cross-feeding, because subsequent products of the methane oxidation pathway, such as methanol, represent alternative carbon sources. We established cocultures in a microcosm model system to determine the mechanism and substrate that underlay the observed cross-feeding in the environment. Lanthanum, a rare earth element, was applied because of its increasing importance in methylotrophy. We used co-occurring strains isolated from Lake Washington sediment that are involved in methane utilization: a methanotroph and two nonmethanotrophic methylotrophs. Gene-expression profiles and mutant analyses suggest that methanol is the dominant carbon and energy source the methanotroph provides to support growth of the nonmethanotrophs. However, in the presence of the nonmethanotroph, gene expression of the dominant methanol dehydrogenase (MDH) shifts from the lanthanide-dependent MDH (XoxF)-type, to the calcium-dependent MDH (MxaF)-type. Correspondingly, methanol is released into the medium only when the methanotroph expresses the MxaF-type MDH. These results suggest a cross-feeding mechanism in which the nonmethanotrophic partner induces a change in expression of methanotroph MDHs, resulting in release of methanol for its growth. This partner-induced change in gene expression that benefits the partner is a paradigm for microbial interactions that cannot be observed in studies of pure cultures, underscoring the importance of synthetic microbial community approaches to understand environmental microbiomes. M icrobial communities and their members are part of every ecosystem and drive important biogeochemical processes on Earth (1). They typically comprise a range of phylogenetically and functionally diverse microbes (2) that are structured by biotic and abiotic factors (3) and are entangled through specific interactions in complex networks (4).The significance of microbial communities in diverse ecosystems including the human body is now widely accepted in science and has led to a range of initiatives focused on the world's microbiomes (5, 6). One important goal within these efforts is to understand how microbes interact with each other and the consequences of such interactions at the level of their transcriptomes, proteomes, and metabolomes. For instance, it has been demonstrated that the metabolism of yeast can be transformed by bacteria-induced prions to decrease the release of inhibiting ethanol (7). In another study, an oral biofilm of the genus Streptococcus displayed different transcriptional responses toward the presence of other species in mixed-species cultures (8).Measuring interactions in complex environmental communities is still a difficult task. Laboratory cocultures represent a simplified approach to assessing...

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Section: Discussionsupporting

confidence: 81%

“…In the methanotroph Methylacidiphilum fumariolicum SolV, the affinity for methanol of XoxF-type MDH was much higher than reported for other MDHs, with a K m of 0.8 μM (40). If the same is true in M. tundripaludum 31/32, the lower affinity of the MxaF-type MDH could result in methanol excretion.…”

Section: Discussionmentioning

confidence: 75%

Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions

Krause

Johnson

Karunaratne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

161

144

View full text Add to dashboard Cite

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“…Also present are genes for the lanthanide-dependent (xoxF) methanol dehydrogenase involved in methanol oxidation to formaldehyde, NAD(P)-dependent methylene-H 4 MPT dehydrogenase (mtd) involved in formaldehyde oxidation to formate, and formate dehydrogenase (fdh) for formate oxidation to CO 2 . The presence of XoxF type methanol dehydrogenases, but absence of the calcium-dependent MxaF type, has also been reported for pelagic non-methanotrophic methylotrophs with relatively small genomes (Giovannoni et al, 2008) and is consistent with recent studies suggesting the prevalence of XoxF compared to MxaF in natural systems (Keltjens et al, 2014;Ramachandran and Walsh, 2015).…”

Section: Recovery Of the Genome Of An Opu3-like Methanotrophic Denitrsupporting

confidence: 75%

Metagenomic Binning Recovers a Transcriptionally Active Gammaproteobacterium Linking Methanotrophy to Partial Denitrification in an Anoxic Oxygen Minimum Zone

et al. 2017

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Diverse planktonic microorganisms play a crucial role in mediating methane flux from the ocean to the atmosphere. The distribution and composition of the marine methanotroph community is determined partly by oxygen availability. The low oxygen conditions of oxygen minimum zones (OMZs) may select for methanotrophs that oxidize methane using inorganic nitrogen compounds (e.g., nitrate, nitrite) in place of oxygen. However, environmental evidence for methane-nitrogen linkages in OMZs remains sparse, as does our knowledge of the genomic content and metabolic capacity of organisms catalyzing OMZ methane oxidation. Here, binning of metagenome sequences from a coastal anoxic OMZ recovered the first near complete (95%) draft genome representing the methanotroph clade OPU3. Phylogenetic reconstruction of concatenated single copy marker genes confirmed the OPU3-like bacterium as a divergent member of the type Ia methanotrophs, with an estimated genome size half that of other sequenced taxa in this group. The proportional abundance of this bacterium peaked at 4% of the total microbial community at the top of the anoxic zone in areas of nitrite and nitrate availability but low methane concentrations. Genes mediating dissimilatory nitrate and nitrite reduction were identified in the OPU3 genome, and transcribed in conjunction with key enzymes catalyzing methane oxidation to formaldehyde and the ribulose monophosphate (RuMP) pathway for formaldehyde assimilation, suggesting partial denitrification linked to methane oxidation. Together, these data provide the first field-based evidence for methanotrophic partial denitrification by the OPU3 cluster under anoxic conditions, supporting a role for OMZs as key sites in pelagic methane turnover.

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“…In addition, they use the rare coenzyme pyrroloquinoline quinone (PQQ). The xoxF gene is clustered with genes for the periplasmic protein XoxJ and the cytochrome c homolog XoxG, a genome context also known from other xoxF homologs (28). These data strongly suggest that Ca.…”

Section: Resultsmentioning

confidence: 52%

“…This finding is typical for methylotrophic organisms, such as Methylobacterium extorquens (27). Intrigued by this result, we constructed a phylogenetic tree of the candidate MDH proteins together with known MDHs classified by Keltjens et al (28). Both Ca.…”

Section: Resultsmentioning

confidence: 99%

Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges

Lackner

Peters

Helfrich

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

126

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The as-yet uncultured filamentous bacteria "Candidatus Entotheonella factor" and "Candidatus Entotheonella gemina" live associated with the marine sponge Theonella swinhoei Y, the source of numerous unusual bioactive natural products. Belonging to the proposed candidate phylum "Tectomicrobia," Candidatus Entotheonella members are only distantly related to any cultivated organism. The Ca. E. factor has been identified as the source of almost all polyketide and modified peptides families reported from the sponge host, and both Ca. Entotheonella phylotypes contain numerous additional genes for as-yet unknown metabolites. Here, we provide insights into the biology of these remarkable bacteria using genomic, (meta)proteomic, and chemical methods. The data suggest a metabolic model of Ca. Entotheonella as facultative anaerobic, organotrophic organisms with the ability to use methanol as an energy source. The symbionts appear to be auxotrophic for some vitamins, but have the potential to produce most amino acids as well as rare cofactors like coenzyme F 420 . The latter likely accounts for the strong autofluorescence of Ca. Entotheonella filaments. A large expansion of protein families involved in regulation and conversion of organic molecules indicates roles in host-bacterial interaction. In addition, a massive overrepresentation of members of the luciferase-like monooxygenase superfamily points toward an important role of these proteins in Ca. Entotheonella. Furthermore, we performed mass spectrometric imaging combined with fluorescence in situ hybridization to localize Ca. Entotheonella and some of the bioactive natural products in the sponge tissue. These metabolic insights into a new candidate phylum offer hints on the targeted cultivation of the chemically most prolific microorganisms known from microbial dark matter.

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PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference

Cited by 333 publications

References 135 publications

Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions

Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions

Metagenomic Binning Recovers a Transcriptionally Active Gammaproteobacterium Linking Methanotrophy to Partial Denitrification in an Anoxic Oxygen Minimum Zone

Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges

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