Biotic Interactions in Microbial Communities as Modulators of Biogeochemical Processes: Methanotrophy as a Model System

Abstract

Microbial interaction is an integral component of microbial ecology studies, yet the role, extent, and relevance of microbial interaction in community functioning remains unclear, particularly in the context of global biogeochemical cycles. While many studies have shed light on the physico-chemical cues affecting specific processes, (micro)biotic controls and interactions potentially steering microbial communities leading to altered functioning are less known. Yet, recent accumulating evidence suggests that the concerted actions of a community can be significantly different from the combined effects of individual microorganisms, giving rise to emergent properties. Here, we exemplify the importance of microbial interaction for ecosystem processes by analysis of a reasonably well-understood microbial guild, namely, aerobic methane-oxidizing bacteria (MOB). We reviewed the literature which provided compelling evidence for the relevance of microbial interaction in modulating methane oxidation. Support for microbial associations within methane-fed communities is sought by a re-analysis of literature data derived from stable isotope probing studies of various complex environmental settings. Putative positive interactions between active MOB and other microbes were assessed by a correlation network-based analysis with datasets covering diverse environments where closely interacting members of a consortium can potentially alter the methane oxidation activity. Although, methanotrophy is used as a model system, the fundamentals of our postulations may be applicable to other microbial guilds mediating other biogeochemical processes.

Incorporating phylogenetic metrics to microbial co‐occurrence networks based on amplicon sequences to discern community assembly processes

“…An essential question in understanding co‐occurrence patterns is identifying the ecological mechanisms that underlie species co‐existence and mutual exclusion. Microbial co‐occurrence networks, mainly reconstructed from amplicon sequencing data, are being increasingly used to infer significant associations between pairs of co‐occurring taxa and often ascribed to biological interactions (Faust & Raes, ; Fuhrman, Cram, & Needham, ; Ho et al, ; Pérez‐Valera et al, ). Critical voices, however, call for caution when analysing and interpreting co‐occurrence networks in order to avoid the description of ecologically meaningless interactions (Barner et al, ; Connor, Barberán, & Clauset, ; Freilich et al, ).…”

Below‐ground connections underlying above‐ground food production: a framework for optimising ecological connections in the rhizosphere

“…Specifically, pathogen success was lower when resident networks had low nestedness (or modularity, see Box 1) and high connectance, presumably through more efficient consumption of resources. Other recent studies found that associations between methane oxidising bacteria and other microbes were central in modulating methane-oxidation (Ho et al 2016), and that fungal co-occurrence network structure was strongly associated with different stages of litter decomposition (Purahong et al 2016). Thus, new ecological knowledge of the structure of interactive networks among organisms and their environment might be used as an indicator of their functional attributes.…”

“…Other recent studies found that associations between methane oxidising bacteria and other microbes were central in modulating methane‐oxidation (Ho et al . ), and that fungal co‐occurrence network structure was strongly associated with different stages of litter decomposition (Purahong et al . ).…”

Experimental erosion of microbial diversity decreases soil CH4consumption rates

“…Methanotroph diversity may buffer ecosystem functioning during environmental fluctuations [58][59][60]. Methanotrophs isolated from environmental samples typically exhibit distinct temperature optima.…”

“…In natural systems, the diversity of even remote taxa often co-varies [10,61], so that BEF relationships observed in such systems reflect the compound effects of diversity changes across multiple, potentially interacting, taxonomic groups. Methanotrophs require other microorganisms for sustained growth [60,62], most likely to remove metabolites that otherwise accumulate to inhibitory levels. Recent experiments also have shown that volatiles produced by heterotrophs, specifically dimethyl sulfides, can promote methanotrophic growth even if heterotrophs are physically isolated [63].…”