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Recovery in methanotrophic activity does not reflect on the methane-driven interaction network after peat mining.

ABSTRACT: Aerobic methanotrophs are crucial in ombrotrophic peatlands, driving the methane and nitrogen cycles. Peat mining adversely affects the methanotrophs, but activity and community composition/abundances may recover after restoration. Considering that the methanotrophic activity and growth are significantly stimulated in the presence of other microorganisms, the methane-driven interaction network, encompassing methanotrophs and non-methanotrophs (i.e., methanotrophic interactome), may also be relevant in conferring community resilience. Yet, little is known of the response and recovery of the methanotrophic interactome to disturbances. Here, we determined the recovery of the methanotrophic interactome as inferred by a co-occurrence network analysis, comparing a pristine and restored peatland. We coupled a DNA-based stable isotope probing (SIP) approach using ¹³C-CH₄ to a co-occurrence network analysis derived from the ¹³C-enriched 16S rRNA gene sequences to relate the response in methanotrophic activity to the structuring of the interaction network. Methanotrophic activity and abundances recovered after peat restoration since 2000. 'Methylomonaceae' was the predominantly active methanotrophs in both peatlands, but differed in the relative abundance of Methylacidiphilaceae and Methylocystis However, bacterial community composition was distinct in both peatlands. Likewise, the methanotrophic interactome was profoundly altered in the restored peatland. Structuring of the interaction network after peat mining resulted in the loss of complexity and modularity, indicating a less connected and efficient network, which may have consequences in the event of recurring/future disturbances. Therefore, determining the response of the methane-driven interaction network, in addition to relating methanotrophic activity to community composition/abundances, provided a more comprehensive understanding of the resilience of the methanotrophs.Importance The resilience and recovery of microorganisms from disturbances are often determined with regard to their activity and community composition/abundances. Rarely has the response of the network of interacting microorganisms been considered, despite accumulating evidence showing that microbial interaction modulates community functioning. Comparing the methane-driven interaction network of a pristine and restored peatland, our findings revealed that the metabolically active microorganisms were less connected and formed less modular 'hubs' in the restored peatland, indicative of a less complex network which may have consequences with recurring disturbances and environmental changes. This also suggests that the resilience and full recovery in the methanotrophic activity and abundances do not reflect on the interaction network. Therefore, it is relevant to consider the interaction-induced response, in addition to documenting changes in activity and community composition/abundances, to provide a comprehensive understanding of the resilience of microorganisms to disturbances.

SUBMITTER: Kaupper T

PROVIDER: S-EPMC8090869 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundBiological interaction affects diverse facets of microbial life by modulating the activity, diversity, abundance, and composition of microbial communities. Aerobic methane oxidation is a community function, with emergent community traits arising from the interaction of the methane-oxidizers (methanotrophs) and non-methanotrophs. Yet little is known of the spatial and temporal organization of these interaction networks in naturally-occurring complex communities. We hypothesized that the assembled bacterial community of the interaction network in methane hotspots would converge, driven by high substrate availability that favors specific methanotrophs, and in turn influences the recruitment of non-methanotrophs. These environments would also share more co-occurring than site-specific taxa.ResultsWe applied stable isotope probing (SIP) using 13C-CH4 coupled to a co-occurrence network analysis to probe trophic interactions in widespread methane-emitting environments, and over time. Network analysis revealed predominantly unique co-occurring taxa from different environments, indicating distinctly co-evolved communities more strongly influenced by other parameters than high methane availability. Also, results showed a narrower network topology range over time than between environments. Co-occurrence pattern points to Chthoniobacter as a relevant yet-unrecognized interacting partner particularly of the gammaproteobacterial methanotrophs, deserving future attention. In almost all instances, the networks derived from the 13C-CH4 incubation exhibited a less connected and complex topology than the networks derived from the unlabelledC-CH4 incubations, likely attributable to the exclusion of the inactive microbial population and spurious connections; DNA-based networks (without SIP) may thus overestimate the methane-dependent network complexity.ConclusionWe demonstrated that site-specific environmental parameters more strongly shaped the co-occurrence of bacterial taxa than substrate availability. Given that members of the interactome without the capacity to oxidize methane can exert interaction-induced effects on community function, understanding the co-occurrence pattern of the methane-driven interaction network is key to elucidating community function, which goes beyond relating activity to community composition, abundances, and diversity. More generally, we provide a methodological strategy that substantiates the ecological linkages between potentially interacting microorganisms with broad applications to elucidate the role of microbial interaction in community function.

Project description:Ombrotrophic peatlands are a recognized global carbon reservoir. Without restoration and peat regrowth, harvested peatlands are dramatically altered, impairing their carbon sink function, with consequences for methane turnover. Previous studies determined the impact of commercial mining on the physicochemical properties of peat and the effects on methane turnover. However, the response of the underlying microbial communities catalyzing methane production and oxidation have so far received little attention. We hypothesize that with the return of Sphagnum spp. postharvest, methane turnover potential and the corresponding microbial communities will converge in a natural and restored peatland. To address our hypothesis, we determined the potential methane production and oxidation rates in natural (as a reference), actively mined, abandoned, and restored peatlands over two consecutive years. In all sites, the methanogenic and methanotrophic population sizes were enumerated using quantitative PCR (qPCR) assays targeting the mcrA and pmoA genes, respectively. Shifts in the community composition were determined using Illumina MiSeq sequencing of the mcrA gene and a pmoA-based terminal restriction fragment length polymorphism (t-RFLP) analysis, complemented by cloning and sequence analysis of the mmoX gene. Peat mining adversely affected methane turnover potential, but the rates recovered in the restored site. The recovery in potential activity was reflected in the methanogenic and methanotrophic abundances. However, the microbial community composition was altered, being more pronounced for the methanotrophs. Overall, we observed a lag between the recovery of the methanogenic/methanotrophic activity and the return of the corresponding microbial communities, suggesting that a longer duration (>15 years) is needed to reverse mining-induced effects on the methane-cycling microbial communities.IMPORTANCE Ombrotrophic peatlands are a crucial carbon sink, but this environment is also a source of methane, an important greenhouse gas. Methane emission in peatlands is regulated by methane production and oxidation catalyzed by methanogens and methanotrophs, respectively. Methane-cycling microbial communities have been documented in natural peatlands. However, less is known of their response to peat mining and of the recovery of the community after restoration. Mining exerts an adverse impact on potential methane production and oxidation rates and on methanogenic and methanotrophic population abundances. Peat mining also induced a shift in the methane-cycling microbial community composition. Nevertheless, with the return of Sphagnum spp. in the restored site after 15 years, methanogenic and methanotrophic activity and population abundance recovered well. The recovery, however, was not fully reflected in the community composition, suggesting that >15 years are needed to reverse mining-induced effects.

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Recovery in methanotrophic activity does not reflect on the methane-driven interaction network after peat mining.

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