skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: 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.  more » « less
Award ID(s):
1847684
PAR ID:
10208144
Author(s) / Creator(s):
; ; ; ; ; ;
Editor(s):
Lloyd, Karen G.
Date Published:
Journal Name:
mSystems
Volume:
5
Issue:
2
ISSN:
2379-5077
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Background Microbial colonization of subsurface shales following hydraulic fracturing offers the opportunity to study coupled biotic and abiotic factors that impact microbial persistence in engineered deep subsurface ecosystems. Shale formations underly much of the continental USA and display geographically distinct gradients in temperature and salinity. Complementing studies performed in eastern USA shales that contain brine-like fluids, here we coupled metagenomic and metabolomic approaches to develop the first genome-level insights into ecosystem colonization and microbial community interactions in a lower-salinity, but high-temperature western USA shale formation. Results We collected materials used during the hydraulic fracturing process (i.e., chemicals, drill muds) paired with temporal sampling of water produced from three different hydraulically fractured wells in the STACK ( S ooner T rend A nadarko Basin, C anadian and K ingfisher) shale play in OK, USA. Relative to other shale formations, our metagenomic and metabolomic analyses revealed an expanded taxonomic and metabolic diversity of microorganisms that colonize and persist in fractured shales. Importantly, temporal sampling across all three hydraulic fracturing wells traced the degradation of complex polymers from the hydraulic fracturing process to the production and consumption of organic acids that support sulfate- and thiosulfate-reducing bacteria. Furthermore, we identified 5587 viral genomes and linked many of these to the dominant, colonizing microorganisms, demonstrating the key role that viral predation plays in community dynamics within this closed, engineered system. Lastly, top-side audit sampling of different source materials enabled genome-resolved source tracking, revealing the likely sources of many key colonizing and persisting taxa in these ecosystems. Conclusions These findings highlight the importance of resource utilization and resistance to viral predation as key traits that enable specific microbial taxa to persist across fractured shale ecosystems. We also demonstrate the importance of materials used in the hydraulic fracturing process as both a source of persisting shale microorganisms and organic substrates that likely aid in sustaining the microbial community. Moreover, we showed that different physicochemical conditions (i.e., salinity, temperature) can influence the composition and functional potential of persisting microbial communities in shale ecosystems. Together, these results expand our knowledge of microbial life in deep subsurface shales and have important ramifications for management and treatment of microbial biomass in hydraulically fractured wells. 
    more » « less
  2. Community assembly describes how different ecological processes shape microbial community composition and structure. How environmental factors impact community assembly remains elusive. Here we sampled microbial communities and >200 biogeochemical variables in groundwater at the Oak Ridge Field Research Center, a former nuclear waste disposal site, and developed a theoretical framework to conceptualize the relationships between community assembly processes and environmental stresses. We found that stochastic assembly processes were critical (>60% on average) in shaping community structure, but their relative importance decreased as stress increased. Dispersal limitation and ‘drift’ related to random birth and death had negative correlations with stresses, whereas the selection processes leading to dissimilar communities increased with stresses, primarily related to pH, cobalt and molybdenum. Assembly mechanisms also varied greatly among different phylogenetic groups. Our findings highlight the importance of microbial dispersal limitation and environmental heterogeneity in ecosystem restoration and management. 
    more » « less
  3. Theoretical frameworks of terrestrial community assembly often focus on single trophic levels (e.g. plants) without considering how complex interdependencies across different trophic levels influence assembly mechanisms. Yet, when multiple trophic levels are considered (e.g. plant–pollinator, plant–microbe interactions) the focus is typically on network analyses at local spatial scales. As spatial variation in biodiversity (β‐diversity) is increasingly being recognized for its relevance in understanding community assembly and conservation, considering how β‐diversity at one trophic level may be influenced by assembly processes that alter abundance and composition of interacting communities at a different trophic level (multitrophic dependency) is critical. Here, we build on single trophic level community assembly frameworks to explore the assembly processes affecting β‐diversity in multitrophic communities comprising flowering plants, their bee pollinators, and the corresponding bee‐gut microbiota to better understand the importance of multitrophic dependency in community assembly. Using distance‐based redundancy analysis and variation partitioning, we investigated community assembly processes across three interconnected trophic levels in two ecological regions in southern California: the Santa Monica Mountains and three islands of the Channel Island Archipelago. We found that the deterministic effects of multitrophic dependency are stronger on directly connected trophic levels than on indirectly connected trophic levels (i.e. flowers explain bee communities and bees explain bee‐gut bacteria communities, but flowers weakly explain variation in bee‐gut bacteria communities). We also found notable regional variation, where multitrophic dependency was weaker on the Channel Islands as ecological drift was more pronounced. Our results suggest that integrating the influence of multitrophic dependency on community assembly is important for elucidating drivers of β‐diversity and that multitrophic dependency can be determined by the regional context in which β‐diversity is measured. Taken together, our results highlight the importance of considering multiscale perspectives – both multitrophic and multiregional – in community assembly to fully elucidate assembly processes. 
    more » « less
  4. Summary The study of islands has made substantial contributions to the development of evolutionary and ecological theory. However, we know little about microbial community assembly on islands. Using soil microbial data collected from 29 lake islands and nearby mainland, we examined the assembly mechanisms of soil bacterial and fungal communities among and within islands. We found that deterministic processes, especially homogeneous selection, tended to be more important in shaping the assembly of soil bacterial communities among islands, while stochastic processes tended to be more important within islands. Moreover, increasing island area increased the importance of homogeneous selection, but reduced the importance of variable selection, for soil bacterial community assembly within islands. By contrast, stochastic processes tended to dominate soil fungal community assembly both among and within islands, with dispersal limitation playing a more important role within than among islands. Our results highlight the scale‐ and taxon‐dependence of insular soil microbial community assembly, suggesting that spatial scale should be explicitly considered when evaluating the influences of habitat fragmentation on soil microbial communities. 
    more » « less
  5. Abstract BackgroundRock-dwelling microorganisms are key players in ecosystem functioning of Antarctic ice free-areas. Yet, little is known about their diversity and ecology, and further still, viruses in these communities have been largely unexplored despite important roles related to host metabolism and nutrient cycling. To begin to address this, we present a large-scale viral catalog from Antarctic rock microbial communities. ResultsWe performed metagenomic analyses on rocks from across Antarctica representing a broad range of environmental and spatial conditions, and which resulted in a predicted viral catalog comprising > 75,000 viral operational taxonomic units (vOTUS). We found largely undescribed, highly diverse and spatially structured virus communities which had predicted auxiliary metabolic genes (AMGs) with functions indicating that they may be potentially influencing bacterial adaptation and biogeochemistry. ConclusionThis catalog lays the foundation for expanding knowledge of virosphere diversity, function, spatial ecology, and dynamics in extreme environments. This work serves as a step towards exploring adaptability of microbial communities in the face of a changing climate. 
    more » « less