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Interkingdom interaction: the soil isopod Porcellio scaber stimulates the methane-driven bacterial and fungal interaction.

ABSTRACT: Porcellio scaber (woodlice) are (sub-)surface-dwelling isopods, widely recognized as "soil bioengineers", modifying the edaphic properties of their habitat, and affecting carbon and nitrogen mineralization that leads to greenhouse gas emissions. Yet, the impact of soil isopods on methane-cycling processes remains unknown. Using P. scaber as a model macroinvertebrate in a microcosm study, we determined how the isopod influences methane uptake and the associated interaction network in an agricultural soil. Stable isotope probing (SIP) with ¹³C-methane was combined to a co-occurrence network analysis to directly link activity to the methane-oxidizing community (bacteria and fungus) involved in the trophic interaction. Compared to microcosms without the isopod, P. scaber significantly induced methane uptake, associated to a more complex bacteria-bacteria and bacteria-fungi interaction, and modified the soil nutritional status. Interestingly, ¹³C was transferred via the methanotrophs into the fungi, concomitant to significantly higher fungal abundance in the P. scaber-impacted soil, indicating that the fungal community utilized methane-derived substrates in the food web along with bacteria. Taken together, results showed the relevance of P. scaber in modulating methanotrophic activity with implications for bacteria-fungus interaction.

SUBMITTER: Heffner T

PROVIDER: S-EPMC10290665 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Interkingdom interaction: the soil isopod Porcellio scaber stimulates the methane-driven bacterial and fungal interaction.

Heffner Tanja T Brami Semi A SA Mendes Lucas W LW Kaupper Thomas T Hannula Emilia S ES Poehlein Anja A Horn Marcus A MA Ho Adrian A

ISME communications 20230624 1

Porcellio scaber (woodlice) are (sub-)surface-dwelling isopods, widely recognized as "soil bioengineers", modifying the edaphic properties of their habitat, and affecting carbon and nitrogen mineralization that leads to greenhouse gas emissions. Yet, the impact of soil isopods on methane-cycling processes remains unknown. Using P. scaber as a model macroinvertebrate in a microcosm study, we determined how the isopod influences methane uptake and the associated interaction network in an agricultu ...[more]

PMID: 37355679

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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:During development, cells may adjust their size to balance between the tissue metabolic demand and the oxygen and resource supply: Small cells may effectively absorb oxygen and nutrients, but the relatively large area of the plasma membrane requires costly maintenance. Consequently, warm and hypoxic environments should favor ectotherms with small cells to meet increased metabolic demand by oxygen supply. To test these predictions, we compared cell size (hindgut epithelium, hepatopancreas B cells, ommatidia) in common rough woodlice (Porcellio scaber) that were developed under four developmental conditions designated by two temperatures (15 or 22°C) and two air O2 concentrations (10% or 22%). To test whether small-cell woodlice cope better under increased metabolic demand, the CO2 production of each woodlouse was measured under cold, normoxic conditions and under warm, hypoxic conditions, and the magnitude of metabolic increase (MMI) was calculated. Cell sizes were highly intercorrelated, indicative of organism-wide mechanisms of cell cycle control. Cell size differences among woodlice were largely linked with body size changes (larger cells in larger woodlice) and to a lesser degree with oxygen conditions (development of smaller cells under hypoxia), but not with temperature. Developmental conditions did not affect MMI, and contrary to predictions, large woodlice with large cells showed higher MMI than small woodlice with small cells. We also observed complex patterns of sexual difference in the size of hepatopancreatic cells and the size and number of ommatidia, which are indicative of sex differences in reproductive biology. We conclude that existing theories about the adaptiveness of cell size do not satisfactorily explain the patterns in cell size and metabolic performance observed here in P. scaber. Thus, future studies addressing physiological effects of cell size variance should simultaneously consider different organismal elements that can be involved in sustaining the metabolic demands of tissue, such as the characteristics of gas-exchange organs and O2-binding proteins.

Project description:Plant root-associated microbiomes play critical roles in promoting plant health, productivity, and tolerance to biotic/abiotic stresses. Blueberry (Vaccinium spp.) is adapted to acidic soils, while the interactions of the root-associated microbiomes in this specific habitat under various root microenvironments remain elusive. Here, we investigated the diversity and community composition of bacterial and fungal communities in various blueberry root niches (bulk soil, rhizosphere soil, and root endosphere). The results showed that blueberry root niches significantly affected root-associated microbiome diversity and community composition compared to those of the three host cultivars. Deterministic processes gradually increased along the soil-rhizosphere-root continuum in both bacterial and fungal communities. The co-occurrence network topological features showed that both bacterial and fungal community complexity and intensive interactions decreased along the soil-rhizosphere-root continuum. Different compartment niches clearly influenced bacterial-fungal interkingdom interactions, which were significantly higher in the rhizosphere, and positive interactions gradually dominated the co-occurrence networks from the bulk soil to the endosphere. The functional predictions showed that rhizosphere bacterial and fungal communities may have higher cellulolysis and saprotrophy capacities, respectively. Collectively, the root niches not only affected microbial diversity and community composition but also enhanced the positive interkingdom interactions between bacterial and fungal communities along the soil-rhizosphere-root continuum. This provides an essential basis for manipulating synthetic microbial communities for sustainable agriculture. IMPORTANCE The blueberry root-associated microbiome plays an essential role in its adaptation to acidic soils and in limiting the uptake of soil nutrients by its poor root system. Studies on the interactions of the root-associated microbiome in the various root niches may deepen our understanding of the beneficial effects in this particular habitat. Our study extended the research on the diversity and composition of microbial communities in different blueberry root compartment niches. Root niches dominated the root-associated microbiome compared to that of the host cultivar, and deterministic processes increased from the bulk soil to the endosphere. In addition, bacterial-fungal interkingdom interactions were significantly higher in the rhizosphere, and those positive interactions progressively dominated the co-occurrence network along the soil-rhizosphere-root continuum. Collectively, root niches dominantly affected the root-associated microbiome and the positive interkingdom interactions increased, potentially providing benefits for the blueberry.

Dataset Information

Interkingdom interaction: the soil isopod Porcellio scaber stimulates the methane-driven bacterial and fungal interaction.

Publications

Interkingdom interaction: the soil isopod Porcellio scaber stimulates the methane-driven bacterial and fungal interaction.

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