A methane‐driven microbial food web in a wetland rice soil

Murase, Jun; Frenzel, Peter

doi:10.1111/j.1462-2920.2007.01414.x

Cited by 98 publications

(100 citation statements)

References 47 publications

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“…Our results suggest that the partner-induced change in gene expression induces the methanotroph to perform a less efficient, leaky function with the result of sustaining the nonmethanotrophic methylotrophic population in the coculture. This methanotrophbased cross-feeding mechanism supports previous results showing that methanotrophs support nonmethanotrophs in natural communities by providing methane-derived carbon (43)(44)(45). Hence, this lanthanum-dependent cross-feeding has the potential to be an important mechanism in the environment.…”

Section: Discussionsupporting

confidence: 70%

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.

147

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: 70%

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.

147

144

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“…Previous experiments with gradient microcosms have already shown that focusing on the active layer allows processes and interactions to be analyzed in unparalleled detail (Murase and Frenzel, 2007;Krause et al, 2010). While only 3 mm thick, the soil layer in the microcosm was considerably thinner and allowed a stronger focus on the organisms of interest than in many other experiments (Dumont et al, 2011, Siljanen et al, 2011.…”

Section: Discussionmentioning

confidence: 93%

“…Recently developed microelectrodes (Revsbech et al, 2009;Revsbech et al, 2011) have demonstrated nanomolar oxygen concentrations in areas that have been considered anoxic so far. However, the design of our microcosms includes a trap to remove any oxygen that might have diffused into the lower compartment (Murase and Frenzel, 2007). Hence, oxygen may have been present in trace amounts in the methane-rich 'anoxic' zone below the oxicanoxic interface, but diffusive transport of oxygen to MOB must have been negligible, if it occurred at all.…”

Section: High-resolution Spatial Analysis Of Methanotrophs a Reim Et Almentioning

confidence: 99%

“…The construction and setup of the microcosms have been described previously (Murase and Frenzel, 2007). Briefly, 14 g dry rice field soil from Vercelli (Italy) was saturated with 7 ml demineralized water and incubated on a polytetrafluoroethylene membrane, which divided the microcosm into an upper and a lower compartment.…”

Section: Soil Microcosm Incubation and Samplingmentioning

confidence: 99%

“…With MOB, these are primarily the counter-gradients of oxygen and methane (Gilbert and Frenzel, 1998). We constructed microcosms that allow incubation of the top 3-mm of a watersaturated soil at near in situ conditions (Murase and Frenzel, 2007). When methane was supplied from below and air was supplied from above, a functioning methanotrophic community developed within a few days, oxidizing virtually all the methane that otherwise would have passed through this soil layer.…”

Section: Introductionmentioning

confidence: 99%

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One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic–anoxic interface in a flooded paddy soil

et al. 2012

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Aerobic methane-oxidizing bacteria (MOB) use a restricted substrate range, yet >30 species-equivalent operational taxonomical units (OTUs) are found in one paddy soil. How these OTUs physically share their microhabitat is unknown. Here we highly resolved the vertical distribution of MOB and their activity. Using microcosms and cryosectioning, we sub-sampled the top 3-mm of a water-saturated soil at near in situ conditions in 100-μm steps. We assessed the community structure and activity using the particulate methane monooxygenase gene pmoA as a functional and phylogenetic marker by terminal restriction fragment length polymorphism (t-RFLP), a pmoA-specific diagnostic microarray, and cloning and sequencing. pmoA genes and transcripts were quantified using competitive reverse transcriptase PCR combined with t-RFLP. Only a subset of the methanotroph community was active. Oxygen microprofiles showed that 89% of total respiration was confined to a 0.67-mm-thick zone immediately above the oxic–anoxic interface, most probably driven by methane oxidation. In this zone, a Methylobacter-affiliated OTU was highly active with up to 18 pmoA transcripts per cell and seemed to be adapted to oxygen and methane concentrations in the micromolar range. Analysis of transcripts with a pmoA-specific microarray found a Methylosarcina-affiliated OTU associated with the surface zone. High oxygen but only nanomolar methane concentrations at the surface suggested an adaptation of this OTU to oligotrophic conditions. No transcripts of type II methanotrophs (Methylosinus, Methylocystis) were found, which indicated that this group was represented by resting stages only. Hence, different OTUs within a single guild shared the same microenvironment and exploited different niches.

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