Ecological Assembly Processes Are Coordinated between Bacterial and Viral Communities in Fractured Shale Ecosystems

Abstract

The ecological drivers that concurrently act upon both a virus and its host and that drive community assembly are poorly understood despite known interactions between viral populations and their microbial hosts. Hydraulically fractured shale environments provide access to a closed ecosystem in the deep subsurface where constrained microbial and viral community assembly processes can be examined. Here, we used metagenomic analyses of time-resolved-produced fluid samples from two wells in the Appalachian Basin to track viral and host dynamics and to investigate community assembly processes. Hypersaline conditions within these ecosystems should drive microbial community structure to a similar configuration through time in response to common osmotic stress. However, viral predation appears to counterbalance this potentially strong homogeneous selection and pushes the microbial community toward undominated assembly. In comparison, while the viral community was also influenced by substantial undominated processes, it assembled, in part, due to homogeneous selection. When the overall assembly processes acting upon both these communities were directly compared with each other, a significant relationship was revealed, suggesting an association between microbial and viral community development despite differing selective pressures. These results reveal a potentially important balance of ecological dynamics that must be in maintained within this deep subsurface ecosystem in order for the microbial community to persist over extended time periods. More broadly, this relationship begins to provide knowledge underlying metacommunity development across trophic levels. IMPORTANCE Interactions between viral communities and their microbial hosts have been the subject of many recent studies in a wide range of ecosystems. The degree of coordination between ecological assembly processes influencing viral and microbial communities, however, has been explored to a much lesser degree. By using a combined null modeling approach, this study investigated the ecological assembly processes influencing both viral and microbial community structure within hydraulically fractured shale environments. Among other results, significant relationships between the structuring processes affecting both the viral and microbial community were observed, indicating that ecological assembly might be coordinated between these communities despite differing selective pressures. Within this deep subsurface ecosystem, these results reveal a potentially important balance of ecological dynamics that must be maintained to enable long-term microbial community persistence. More broadly, this relationship begins to provide insight into the development of communities across trophic levels.

Using metacommunity ecology to understand environmental metabolomes

“…Having a common conceptual grounding across studies provides an opportunity to investigate assembly processes affecting metabolite assemblages, and to develop theory that applies across and within ecosystems and spatiotemporal scales. Moreover, this common theory can be used to study ecological communities (e.g., microbes) and the metabolites they transform using the same framework, as previously performed with bacteria and viruses 78 . The degree of coordination between assembly processes can be subsequently related to microbial processes, DOM components, and environmental factors to reveal variables important to convergent and divergent assembly, in turn providing insight into those factors underlying biogeochemistry.…”

“…While we focused heavily on dendrogram-based null models, there are other immediate opportunities to advance understanding by combining dendrogram-based and dendrogram-free null models. This approach has been pioneered in microbial ecology to parse out the relative influences of variable selection, homogeneous selection, dispersal limitation (combined with drift), and homogenizing dispersal (i.e., mass effects) 35 , 64 , 78 , 81 . More specifically, this is pursued by combining the βNTI null model with the identity-based Raup–Crick null model.…”

Microbial Communities in a Serpentinizing Aquifer Are Assembled through Strong Concurrent Dispersal Limitation and Selection

“…Advances in DNA sequencing technology in the last 2 decades ( 25 ), paired with the more recent implementation of community assembly theory and modeling of sequencing data from microbial ecosystems, have provided new insights into the mechanisms that structure microbial communities in a variety of conditions ( 24 , 26 – 36 ). Assessments of community assembly in groundwater systems have shown that selection and dispersal processes play an extremely important role in structuring both the environmental resource landscape as well as microbial communities ( 29 , 31 , 32 , 34 , 37 ). Due to accessibility, much of this work has been performed in neutral pH, near surface, groundwaters with connectivity to the surface ( 31 , 32 , 37 ).…”

“…Due to accessibility, much of this work has been performed in neutral pH, near surface, groundwaters with connectivity to the surface ( 31 , 32 , 37 ). Relatively little work has been done in isolated hard-rock aquifers within the deep subsurface ( 29 , 34 ). Old groundwaters (>100 years), which are often hosted within hard-rock aquifers in the deep subsurface, are a substantial reservoir of globally available freshwater ( 38 ).…”

“…Old groundwaters (>100 years), which are often hosted within hard-rock aquifers in the deep subsurface, are a substantial reservoir of globally available freshwater ( 38 ). As these systems are likely dispersal limited, it is important that we understand the ecological forces that structure microbial communities in hard-rock aquifers ( 29 , 34 ) to better account for the controls on microbial community composition and function within these large reservoirs of valuable water resources ( 39 ).…”