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.

Keywords: ecosystem functioning; methane oxidation; methanotrophy; microbial interaction; microbial network.

Figure 1

Representative co-occurrence network of OTUs derived from 16 s rRNA gene sequences. The network depicts OTUs classified as MOB together with other OTUs which significantly and positively correlated with them. The OTUs were derived from the “heavy” fraction (i.e., isotopically labeled DNA) of a SIP gradient from a ¹³C–CH₄ labeling experiment of a microbial community in sediments from a geothermal spring (Sharp et al., 2014). Only OTUs with >10 total reads and which appeared in >20% of the samples were taken into account. Full taxonomic affiliation corresponding to the numbers are listed in the Supplementary Information (Table S1). The experimental conditions and site information are given in Table 1.

Figure 2

Biotic interaction as modulator of methane oxidation. Obligate aerobic MOB forms a close-knit community with its biotic component, benefiting from interaction with other microorganisms in the consortium. Yet, aerobic MOB are not dependent on the interacting microorganisms as depicted by a co-dependent partnership. Within the MOB consortia, the level of interaction may oscillate depending on environmental conditions and factors/cues affecting the community network.