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Organic Particles: Heterogeneous Hubs for Microbial Interactions in Aquatic Ecosystems.

ABSTRACT: The dynamics and activities of microbes colonizing organic particles (hereafter particles) greatly determine the efficiency of the aquatic carbon pump. Current understanding is that particle composition, structure and surface properties, determined mostly by the forming organisms and organic matter, dictate initial microbial colonization and the subsequent rapid succession events taking place as organic matter lability and nutrient content change with microbial degradation. We applied a transcriptomic approach to assess the role of stochastic events on initial microbial colonization of particles. Furthermore, we asked whether gene expression corroborates rapid changes in carbon-quality. Commonly used size fractionated filtration averages thousands of particles of different sizes, sources, and ages. To overcome this drawback, we used replicate samples consisting each of 3-4 particles of identical source and age and further evaluated the consequences of averaging 10-1000s of particles. Using flow-through rolling tanks we conducted long-term experiments at near in situ conditions minimizing the biasing effects of closed incubation approaches often referred to as "the bottle-effect." In our open flow-through rolling tank system, however, active microbial communities were highly heterogeneous despite an identical particle source, suggesting random initial colonization. Contrasting previous reports using closed incubation systems, expression of carbon utilization genes didn't change after 1 week of incubation. Consequently, we suggest that in nature, changes in particle-associated community related to carbon availability are much slower (days to weeks) due to constant supply of labile, easily degradable organic matter. Initial, random particle colonization seems to be subsequently altered by multiple organismic interactions shaping microbial community interactions and functional dynamics. Comparative analysis of thousands particles pooled togethers as well as pooled samples suggests that mechanistic studies of microbial dynamics should be done on single particles. The observed microbial heterogeneity and inter-organismic interactions may have important implications for evolution and biogeochemistry in aquatic systems.

SUBMITTER: Bizic-Ionescu M

PROVIDER: S-EPMC6212488 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Organic Particles: Heterogeneous Hubs for Microbial Interactions in Aquatic Ecosystems.

Bižić-Ionescu Mina M Ionescu Danny D Grossart Hans-Peter HP

Frontiers in microbiology 20181026

The dynamics and activities of microbes colonizing organic particles (hereafter particles) greatly determine the efficiency of the aquatic carbon pump. Current understanding is that particle composition, structure and surface properties, determined mostly by the forming organisms and organic matter, dictate initial microbial colonization and the subsequent rapid succession events taking place as organic matter lability and nutrient content change with microbial degradation. We applied a transcri ...[more]

PMID: 30416497

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Project description:In subtropical forest ecosystems with few phosphorus (P) inputs, P availability and forest productivity depend on soil organic P (Po) mineralization. However, the mechanisms by which the microbial community determines the status and fate of soil Po mineralization remain unclear. In the present study, soils were collected from three typical forest types: secondary natural forest (SNF), mixed planting, and monoculture forest of Chinese fir. The P fractions, Po-mineralization ability, and microbial community in the soils of different forest types were characterized. In addition, we defined Po-mineralizing taxa with the potential to interact with the soil microbial community to regulate Po mineralization. We found that a higher labile P content persisted in SNF and was positively associated with the Po-mineralization capacity of the soil microbial community. In vitro cultures of soil suspensions revealed that soil Po mineralization of three forest types was distinguished by differences in the composition of fungal communities. We further identified broad phylogenetic lineages of Po-mineralizing fungi with a high intensity of positive interactions with the soil microbial community, implying that the facilitation of Po-mineralizing taxa is crucial for soil P availability. Our dilution experiments to weaken microbial interactions revealed that in SNF soil, which had the highest interaction intensity of Po-mineralizing taxa with the community, Po-mineralization capacity was irreversibly lost after dilution, highlighting the importance of microbial diversity protection in forest soils. In summary, this study demonstrates that the interactions of Po-mineralizing microorganisms with the soil microbial community are critical for P availability in subtropical forests.IMPORTANCEIn subtropical forest ecosystems with few phosphorus inputs, phosphorus availability and forest productivity depend on soil organic phosphorus mineralization. However, the mechanisms by which the microbial community interactions determine the mineralization of soil organic phosphorus remain unclear. In the present study, soils were collected from three typical forest types: secondary natural forest, mixed planting, and monoculture forest of Chinese fir. We found that a higher soil labile phosphorus content was positively associated with the organic phosphorus mineralization capacity of the soil microbial community. Soil organic phosphorus mineralization of three forest types was distinguished by the differences in the composition of fungal communities. The positive interactions between organic phosphorus-mineralizing fungi and the rest of the soil microbial community facilitated organic phosphorus mineralization. This study highlights the importance of microbial diversity protection in forest soils and reveals the microbial mechanism of phosphorus availability maintenance in subtropical forest ecosystems.

Project description:BackgroundThe sulfur cycle encompasses a series of complex aerobic and anaerobic transformations of S-containing molecules and plays a fundamental role in cellular and ecosystem-level processes, influencing biological carbon transfers and other biogeochemical cycles. Despite their importance, the microbial communities and metabolic pathways involved in these transformations remain poorly understood, especially for inorganic sulfur compounds of intermediate oxidation states (thiosulfate, tetrathionate, sulfite, polysulfides). Isolated and highly stratified, the extreme geochemical and environmental features of meromictic ice-capped Lake A, in the Canadian High Arctic, provided an ideal model ecosystem to resolve the distribution and metabolism of aquatic sulfur cycling microorganisms along redox and salinity gradients.ResultsApplying complementary molecular approaches, we identified sharply contrasting microbial communities and metabolic potentials among the markedly distinct water layers of Lake A, with similarities to diverse fresh, brackish and saline water microbiomes. Sulfur cycling genes were abundant at all depths and covaried with bacterial abundance. Genes for oxidative processes occurred in samples from the oxic freshwater layers, reductive reactions in the anoxic and sulfidic bottom waters and genes for both transformations at the chemocline. Up to 154 different genomic bins with potential for sulfur transformation were recovered, revealing a panoply of taxonomically diverse microorganisms with complex metabolic pathways for biogeochemical sulfur reactions. Genes for the utilization of sulfur cycle intermediates were widespread throughout the water column, co-occurring with sulfate reduction or sulfide oxidation pathways. The genomic bin composition suggested that in addition to chemical oxidation, these intermediate sulfur compounds were likely produced by the predominant sulfur chemo- and photo-oxidisers at the chemocline and by diverse microbial degraders of organic sulfur molecules.ConclusionsThe Lake A microbial ecosystem provided an ideal opportunity to identify new features of the biogeochemical sulfur cycle. Our detailed metagenomic analyses across the broad physico-chemical gradients of this permanently stratified lake extend the known diversity of microorganisms involved in sulfur transformations over a wide range of environmental conditions. The results indicate that sulfur cycle intermediates and organic sulfur molecules are major sources of electron donors and acceptors for aquatic and sedimentary microbial communities in association with the classical sulfur cycle. Video abstract.

Dataset Information

Organic Particles: Heterogeneous Hubs for Microbial Interactions in Aquatic Ecosystems.

Publications

Organic Particles: Heterogeneous Hubs for Microbial Interactions in Aquatic Ecosystems.

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