Minkina, T. M. | bioRxiv Science

bioRxiv2025

Oligotrophy and organic carbon dissipation as trophic strategy in chernozem rare and uncultured taxa

Soil microbial communities harbor vast phylogenetic diversity, yet the functional ecology of rare and uncultured taxa remains poorly understood. These low-abundance microorganisms may employ specialized trophic strategies enabling their persistence in resource-limited environments. This study examined whether established oligotrophy markers could effectively characterize and differentiate the ecophysiology of rare and uncultured bacteria recovered from diverse Russian soil metagenomes. A total of 31 soil samples (chernozems, fluvisols, solonetz, solonchak, kastanozems, and leptosols) were collected from protected natural areas in the Rostov Region, Russia. Shotgun metagenomic sequencing was performed, and 246 metagenome-assembled genomes (MAGs) were recovered through assembly and binning. Genomic and functional traits associated with oligotrophy - including genome size, predicted generation time, ribosomal RNA operon copy number, two-component signaling systems, chemotaxis proteins, and carbohydrate-active enzymes - were analyzed. Metabolic capabilities for C1-compound oxidation, benzoyl-CoA pathway utilization, organosulfonate metabolism, and atmospheric trace gas scavenging were annotated. Principal component analysis was employed to cluster MAGs based on ecological strategy. MAGs spanned 18 bacterial phyla, with genome sizes ranging from 0.58-11.6 Mb and predicted doubling times from 0.6-15.6 hours. Six statistically significant clusters were identified, corresponding to distinct life-history strategies: fast-growing generalists, hydrogenotrophs, C1-compound specialists, polysaccharide degraders, aromatic compound degraders, and minimal-genome specialists. Oligotrophic lifestyles were confidently inferred for Methylomirabilota, Krumholzibacteriota, and Eisenbacteria MAGs, characterized by slow growth, reliance on low-molecular-weight carbon dissipation, and reduced regulatory complexity. Copiotrophic strategies were associated with Myxococcota, Bacteroidota, Gammaproteobacteria, and Verrucomicrobiota, which exhibited large genomes, rapid doubling times, extensive two-component systems, and high carbohydrate-active enzyme abundances. Combined analysis of genome size, generation time, regulatory system complexity, chemotaxis capacity, and substrate utilization pathways provides a robust framework for inferring trophic strategies of uncultured soil bacteria. Oligotrophy among rare taxa is characterized by adaptation to low-molecular-weight carbon dissipation, atmospheric trace gas oxidation, representing ecological strategies that enable persistence in nutrient-limited soil microhabitats.

microbiology↗

bioRxiv2023

Sulfur cycle microbiota in extremely contaminated Technosol with ongoing pedogenesis: culture-dependent and metagenomic approach

Understanding the microbial communities involved in the global sulfur cycle is crucial for comprehending key biogeochemical processes on Earth. However, most studies tend to focus on marine ecosystems, while investigations into the terrestrial sulfur cycle are scarce. In this study, we employed culture-dependent techniques and metagenomics to characterize sulfur-cycling microbiota in extremely contaminated soils. We analyzed shotgun and amplicon sequencing data to assess taxonomical diversity, metagenome-assembled genomes (MAGs) for functional diversity, and also calculated the most probable numbers (MPN) of sulfur-oxidizing and sulfate-reducing bacteria based on culture-dependent data. Our taxonomic profiling, using both shotgun and amplicon data, revealed a high diversity of sulfur cycle bacteria, which was found to be dependent on pH levels. Additionally, our findings confirmed recent modelling of specific taxa biogeographical distribution, such as the sulfur-reducing Mesotoga. Using a functional metagenomics approach, we identified non-canonical taxa involved in dissimilatory sulfur metabolism (e.g., sulfate-reducing acidobacteria and members of the Binatota phylum), and canonical taxa engaged in various oxidative, reductive, and organosulfur transformations (e.g., sulfur-oxidizing alpha-, beta-, and gammaproteobacteria). Furthermore, we discovered that multiple taxa in the studied Technosol encoded different enzymes capable of sulfite transformation and the removal of sulfite from various organosulfonate molecules, thus contributing to the cryptic cycling of sulfur compounds. Estimated MPNs of sulfur-oxidizing bacteria aligned with our shotgun and amplicon data, while those of sulfate-reducing bacteria contradicted functional metagenomic findings. Based on our overall analysis, we support the idea that sulfate-reducers belong to the rare biosphere in soil. We suggest that they behave differently in soils compared to aquatic habitats due to the high taxonomic diversity along with low absolute abundance. Our findings unveil a diverse and unique community of sulfur-metabolizing bacteria that has evolved in soil under severe technogenic pollution, high bulk sulfur content, and fluctuating redox states.

microbiology↗