Methane-fed microbial microcosms show differential community dynamics and pinpoint taxa involved in communal response

Oshkin, Igor Y.; Beck, David A. C.; Lamb, Andrew; Tchesnokova, Veronika; Benuska, Gabrielle; McTaggart, Tami L.; Kalyuzhnaya, Marina G.; Dedysh, Svetlana N.; Lidstrom, Mary E.; Chistoserdova, Ludmila

doi:10.1038/ismej.2014.203

Cited by 130 publications

(186 citation statements)

References 41 publications

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“…M. tundripaludum produces primarily 3-OH-C 10 -HSL, a signal that is also produced by environmental isolates of other bacterial species, including Burkholderia thailandensis (14) and Pseudomonas fluorescens (26). This opens up the possibility of cross talk between bacterial species in methane-oxidizing communities, as both Burkholderiales and pseudomonads have also been identified in enrichments from Lake Washington sediment (3,7).…”

Section: Discussionmentioning

confidence: 93%

“…Methanotrophs provide a carbon and energy source for communities of organisms that cannot oxidize methane themselves, thereby serving as key supporting species in the environment (3,4). The methanotroph Methylobacter tundripaludum is a member of the Gammaproteobacteria (type I methanotroph), and it has been repeatedly identified as a dominant member of methane enrichment and stable isotope probing experiments of sediment from Lake Washington, Seattle, WA (3,(5)(6)(7). Methylobacter spp.…”

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confidence: 99%

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Quorum Sensing in a Methane-Oxidizing Bacterium

Puri

Schaefer

et al. 2017

J Bacteriol

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Aerobic methanotrophic bacteria use methane as their sole source of carbon and energy and serve as a major sink for the potent greenhouse gas methane in freshwater ecosystems. Dissecting the molecular details of how these organisms interact in the environment may increase our understanding of how they perform this important ecological role. Many bacterial species use quorum sensing (QS) systems to regulate gene expression in a cell density-dependent manner. We have identified a QS system in the genome of Methylobacter tundripaludum, a dominant methane oxidizer in methane enrichments of sediment from Lake Washington (Seattle, WA). We determined that M. tundripaludum produces primarily N-3-hydroxydecanoyl-L-homoserine lactone (3-OH-C 10 -HSL) and that its production is governed by a positive feedback loop. We then further characterized this system by determining which genes are regulated by QS in this methane oxidizer using transcriptome sequencing (RNA-seq) and discovered that this system regulates the expression of a putative nonribosomal peptide synthetase biosynthetic gene cluster. Finally, we detected an extracellular factor that is produced by M. tundripaludum in a QS-dependent manner. These results identify and characterize a mode of cellular communication in an aerobic methane-oxidizing bacterium.IMPORTANCE Aerobic methanotrophs are critical for sequestering carbon from the potent greenhouse gas methane in the environment, yet the mechanistic details of chemical interactions in methane-oxidizing bacterial communities are not well understood. Understanding these interactions is important in order to maintain, and potentially optimize, the functional potential of the bacteria that perform this vital ecosystem function. In this work, we identify a quorum sensing system in the aerobic methanotroph Methylobacter tundripaludum and use both chemical and genetic methods to characterize this system at the molecular level.KEYWORDS methane, methanotroph, quorum sensing, sociomicrobiology, acyl-homoserine lactone, biosynthetic gene cluster A erobic methane-oxidizing bacteria (methanotrophs) are an important component of the carbon cycle that serve to sequester carbon from the potent greenhouse gas methane after it is produced by anaerobic microbial ecosystems (1, 2). Methanotrophs provide a carbon and energy source for communities of organisms that cannot oxidize methane themselves, thereby serving as key supporting species in the environment (3, 4). The methanotroph Methylobacter tundripaludum is a member of the Gammaproteobacteria (type I methanotroph), and it has been repeatedly identified as a dominant member of methane enrichment and stable isotope probing experiments of sediment from Lake Washington, Seattle, WA (3, 5-7). Methylobacter spp. have also been isolated from other geographically distinct regions, including the arctic (8), estuaries (9), and temperate wetlands (10), highlighting the diverse environments inhabited by this genus. We, therefore, use M. tundripaludum as part of a model system for ...

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Section: Discussionmentioning

confidence: 93%

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confidence: 99%

Quorum Sensing in a Methane-Oxidizing Bacterium

Puri

Schaefer

et al. 2017

J Bacteriol

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“…The Methylophilaceae types were successfully enriched on either methanol or methylamine, and multiple pure cultures were isolated (Beck et al 2014;McTaggart et al 2015a). While highly enriched cultures of Methylobacter were easy to establish at semi-in situ temperatures (Oshkin et al 2015), pure cultures were extremely difficult to obtain. Most of the cultures remained mixed even after months of incubation and after multiple transfers with dilutions.…”

Section: Recent Insights From Cultivation Approachesmentioning

confidence: 99%

Methylotrophs in natural habitats: current insights through metagenomics

Chistoserdova

2015

Appl Microbiol Biotechnol

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113

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The focus of this review is on the recent data from the omics approaches, measuring the presence of methylotrophs in natural environments. Both Bacteria and Archaea are considered. The data are discussed in the context of the current knowledge on the biochemistry of methylotrophy and the physiology of cultivated methylotrophs. One major issue discussed is the recent metagenomic data pointing toward the activity of "aerobic" methanotrophs, such as Methylobacter, in microoxic or hypoxic conditions. A related issue of the metabolic distinction between aerobic and "anaerobic" methylotrophy is addressed in the light of the genomic and metagenomic data for respective organisms. The role of communities, as opposed to single-organism activities in environmental cycling of single-carbon compounds, such as methane, is also discussed. In addition, the emerging issue of the role of non-traditional methylotrophs in global metabolism of single-carbon compounds and the role of methylotrophy pathways in non-methylotrophs is briefly mentioned.

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“…1). This microcosm model system is based on that used to enrich methane-consuming communities, which resulted in dominance of M. tundripaludum 31/32 and M. mobilis strains similar to those found in sediment (37). Cells were grown with methane under low initial O 2 , with daily headspace replacement and weekly culture transfer to new medium (36).…”

Section: Establishing Cocultures From Isolates As Observed In the Envmentioning

confidence: 99%

“…These isolates originated from Lake Washington sediment (33-35), a freshwater ecosystem, which is characterized by a dynamic turnover of methane (16) and strong co-occurrence patterns of methanotrophs and nonmethanotrophic methylotrophs (36,37). The isolates used are representative of strains that dominate methane-enriched microcosms and 13 C SIP studies of sediment (13).…”

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confidence: 99%

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.

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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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Methane-fed microbial microcosms show differential community dynamics and pinpoint taxa involved in communal response

Cited by 130 publications

References 41 publications

Quorum Sensing in a Methane-Oxidizing Bacterium

Quorum Sensing in a Methane-Oxidizing Bacterium

Methylotrophs in natural habitats: current insights through metagenomics

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

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