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Phagotrophic Protists and Their Associates: Evidence for Preferential Grazing in an Abiotically Driven Soil Ecosystem.

ABSTRACT: The complex relationship between ecosystem function and soil food web structure is governed by species interactions, many of which remain unmapped. Phagotrophic protists structure soil food webs by grazing the microbiome, yet their involvement in intraguild competition, susceptibility to predator diversity, and grazing preferences are only vaguely known. These species-dependent interactions are contextualized by adjacent biotic and abiotic processes, and thus obfuscated by typically high soil biodiversity. Such questions may be investigated in the McMurdo Dry Valleys (MDV) of Antarctica because the physical environment strongly filters biodiversity and simplifies the influence of abiotic factors. To detect the potential interactions in the MDV, we analyzed the co-occurrence among shotgun metagenome sequences for associations suggestive of intraguild competition, predation, and preferential grazing. In order to control for confounding abiotic drivers, we tested co-occurrence patterns against various climatic and edaphic factors. Non-random co-occurrence between phagotrophic protists and other soil fauna was biotically driven, but we found no support for competition or predation. However, protists predominately associated with Proteobacteria and avoided Actinobacteria, suggesting grazing preferences were modulated by bacterial cell-wall structure and growth rate. Our study provides a critical starting-point for mapping protist interactions in native soils and highlights key trends for future targeted molecular and culture-based approaches.

SUBMITTER: Thompson AR

PROVIDER: S-EPMC8398437 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe impact of the microbiota on host fitness has so far mainly been demonstrated for the bacterial microbiome. We know much less about host-associated protist and viral communities, largely due to technical issues. However, all microorganisms within a microbiome potentially interact with each other as well as with the host and the environment, therefore likely affecting the host health.ResultsWe set out to explore how environmental and host factors shape the composition and diversity of bacterial, protist and viral microbial communities in the Pacific oyster hemolymph, both in health and disease. To do so, five oyster families differing in susceptibility to the Pacific oyster mortality syndrome were reared in hatchery and transplanted into a natural environment either before or during a disease outbreak. Using metabarcoding and shotgun metagenomics, we demonstrate that hemolymph can be considered as an ecological niche hosting bacterial, protist and viral communities, each of them shaped by different factors and distinct from the corresponding communities in the surrounding seawater. Overall, we found that hemolymph microbiota is more strongly shaped by the environment than by host genetic background. Co-occurrence network analyses suggest a disruption of the microbial network after transplantation into natural environment during both non-infectious and infectious periods. Whereas we could not identify a common microbial community signature for healthy animals, OsHV-1 μVar virus dominated the hemolymph virome during the disease outbreak, without significant modifications of other microbiota components.ConclusionOur study shows that oyster hemolymph is a complex ecosystem containing diverse bacteria, protists and viruses, whose composition and dynamics are primarily determined by the environment. However, all of these are also shaped by oyster genetic backgrounds, indicating they indeed interact with the oyster host and are therefore not only of transient character. Although it seems that the three microbiome components respond independently to environmental conditions, better characterization of hemolymph-associated viruses could change this picture.

Project description:BackgroundViruses impact nearly all organisms on Earth, including microbial communities and their associated biogeochemical processes. In soils, highly diverse viral communities have been identified, with a global distribution seemingly driven by multiple biotic and abiotic factors, especially soil temperature and moisture. However, our current understanding of the stability of soil viral communities across time and their response to strong seasonal changes in environmental parameters remains limited. Here, we investigated the diversity and activity of environmental soil DNA and RNA viruses, focusing especially on bacteriophages, across dynamics' seasonal changes in a snow-dominated mountainous watershed by examining paired metagenomes and metatranscriptomes.ResultsWe identified a large number of DNA and RNA viruses taxonomically divergent from existing environmental viruses, including a significant proportion of fungal RNA viruses, and a large and unsuspected diversity of positive single-stranded RNA phages (Leviviricetes), highlighting the under-characterization of the global soil virosphere. Among these, we were able to distinguish subsets of active DNA and RNA phages that changed across seasons, consistent with a "seed-bank" viral community structure in which new phage activity, for example, replication and host lysis, is sequentially triggered by changes in environmental conditions. At the population level, we further identified virus-host dynamics matching two existing ecological models: "Kill-The-Winner" which proposes that lytic phages are actively infecting abundant bacteria, and "Piggyback-The-Persistent" which argues that when the host is growing slowly, it is more beneficial to remain in a dormant state. The former was associated with summer months of high and rapid microbial activity, and the latter with winter months of limited and slow host growth.ConclusionTaken together, these results suggest that the high diversity of viruses in soils is likely associated with a broad range of host interaction types each adapted to specific host ecological strategies and environmental conditions. As our understanding of how environmental and host factors drive viral activity in soil ecosystems progresses, integrating these viral impacts in complex natural microbiome models will be key to accurately predict ecosystem biogeochemistry. Video Abstract.

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Phagotrophic Protists and Their Associates: Evidence for Preferential Grazing in an Abiotically Driven Soil Ecosystem.

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