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

Putman, Lindsay I.; Sabuda, Mary; Brazelton, William J.; Kubo, M. D.; Hoehler, Tori M.; McCollom, T. M.; Cardace, D.; Schrenk, M. O.

doi:10.1128/msystems.00300-21

Cited by 17 publications

(16 citation statements)

References 85 publications

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“…Indeed, there are active microbial ecosystems in the deep subsurface fueled by serpentinization (reviewed previously in Schrenk et al, 2013 ). The origin of microorganisms within these subsurface communities is thought to be related to transportation to the subsurface during ophiolite obduction or introduction from groundwater along slow regional flow pathways ( Sabuda et al, 2020 ; Putman et al, 2021 ). Microbial communities dependent on serpentinization are of particular interest to theories of the origin of life and potential life elsewhere in the solar system such as Mars or icy moons (e.g., Schulte et al, 2006 ; Martin et al, 2008 ; Cardace and Hoehler, 2009 ; Sojo et al, 2016 ; Preiner et al, 2018 ; Cartwright and Russell, 2019 ; Russell and Ponce, 2020 ; Taubner et al, 2020 ).…”

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

“…Recent work utilizes next generation DNA sequencing for taxonomic and functional classification of borehole fluids in combination with other techniques such as microcosm or enrichment based experiments ( Crespo-Medina et al, 2014 ; Meyer-Dombard et al, 2018 ; Fones et al, 2021 ; Glombitza et al, 2021 ), stable isotope analyses ( Nothaft et al, 2021a , b ), radioisotope labeling ( Fones et al, 2021 ; Glombitza et al, 2021 ; Templeton et al, 2021 ), and ecological/hydrological modeling ( Putman et al, 2021 ). Transcriptomic and single cell genomics studies have also shown mechanisms of adaptation of microbial life to serpentinizing environments ( Fones et al, 2019 , 2021 ; Merino et al, 2020 ; Kraus et al, 2021 ).…”

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

“…Microbial communities in fluids most influenced by serpentinization are dominated by Bacteria, with variable archaeal abundances (< 1% to ∼30%), and generally consist of low richness and planktonic cell abundances (≤ 10 6 cells mL –1 ) (e.g., Rempfert et al, 2017 ; Twing et al, 2017 ; Fones et al, 2019 , 2021 ; Kraus et al, 2021 ; Putman et al, 2021 ; Sabuda et al, 2021 ). Studies associated with rock solids in these environments are uncommon, but microscopy and 16S rRNA sequencing from cores obtained during drilling at CROMO and at MBO indicated variable cell abundances (10 3 –10 7 cells per gram) and low taxonomic richness ( Cardace et al, 2013 ; Kelemen et al, 2020 ; Templeton et al, 2021 ).…”

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

“…Studies associated with rock solids in these environments are uncommon, but microscopy and 16S rRNA sequencing from cores obtained during drilling at CROMO and at MBO indicated variable cell abundances (10 3 –10 7 cells per gram) and low taxonomic richness ( Cardace et al, 2013 ; Kelemen et al, 2020 ; Templeton et al, 2021 ). Selective pressures that affect community structure in these environments include low dissolved inorganic carbon (DIC) concentrations, high pH, low dissolved oxygen (DO), and energy limitations ( Rempfert et al, 2017 ; Twing et al, 2017 ; Fones et al, 2019 , 2021 ; Nothaft et al, 2021a ; Putman et al, 2021 ). While microbial populations in highly reducing, hyperalkaline groundwater are generally limited by the lack of more energy rich electron acceptors (oxidants such as O 2 , NO 3 – , and Mn; e.g., Twing et al, 2017 ), this may not be the most important limitation on microbial metabolisms ( Crespo-Medina et al, 2014 ; Rempfert et al, 2017 ; Glombitza et al, 2021 ).…”

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

“…Enrichment experiments show low DIC may be most limiting, driving the selection for unique adaptations such as higher rates of substrate assimilation to dissimilation, and methanogen diversification ( Crespo-Medina et al, 2014 ; Fones et al, 2019 , 2021 ; Kraus et al, 2021 ). Finally, ecological modeling has shown dispersal limitation due to low permeability and slow fluid flow imposes strong selective pressure on microbial communities within ophiolite hosted aquifers at CROMO ( Putman et al, 2021 ), leading to microbial community differentiation.…”

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

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Advances in Defining Ecosystem Functions of the Terrestrial Subsurface Biosphere

Meyer-Dombard

Malas

2022

Front. Microbiol.

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The subsurface is one of the last remaining ‘uncharted territories’ of Earth and is now accepted as a biosphere in its own right, at least as critical to Earth systems as the surface biosphere. The terrestrial deep biosphere is connected through a thin veneer of Earth’s crust to the surface biosphere, and many subsurface biosphere ecosystems are impacted by surface topography, climate, and near surface groundwater movement and represent a transition zone (at least ephemerally). Delving below this transition zone, we can examine how microbial metabolic functions define a deep terrestrial subsurface. This review provides a survey of the most recent advances in discovering the functional and genomic diversity of the terrestrial subsurface biosphere, how microbes interact with minerals and obtain energy and carbon in the subsurface, and considers adaptations to the presented environmental extremes. We highlight the deepest subsurface studies in deep mines, deep laboratories, and boreholes in crystalline and altered host rock lithologies, with a focus on advances in understanding ecosystem functions in a holistic manner.

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Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

Section: Exploring the Terrestrial Deep Biospherementioning

confidence: 99%

See 3 more Smart Citations

Advances in Defining Ecosystem Functions of the Terrestrial Subsurface Biosphere

Meyer-Dombard

Malas

2022

Front. Microbiol.

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Differential microbial assembly processes and co‐occurrence networks in the soil‐root continuum along an environmental gradient

Zhong

Sørensen

Zhu

et al. 2022

iMeta

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Microorganisms of the soil‐root continuum play key roles in ecosystem function. The Loess Plateau is well known for its severe soil erosion and thick loess worldwide, where mean annual precipitation (MAP) and soil nutrients decrease from the southeast to the northwest. However, the relative influence of environmental factors on the microbial community in four microhabitats (bulk soil, rhizosphere, rhizoplane, and endosphere) in the soil‐root continuum along the environmental gradient in the Loess Plateau remains unclear. In this study, we investigated 82 field sites from warm‐temperate to desert grasslands across the Loess Plateau, China, to assess the bacterial diversity, composition, community assembly, and co‐occurrence networks in the soil‐root continuum along an environmental gradient using bacterial 16S recombinant DNA amplicon sequencing. We discovered that the microhabitats explained the largest source of variations in the bacterial diversity and community composition in this region. Environmental factors (e.g., MAP, soil organic carbon, and pH) impacted the soil, rhizosphere, and rhizoplane bacterial communities, but their effects on the bacterial community decreased with increased proximity to roots from the soil to the rhizoplane, and the MAP enlarged the dissimilarity of microbial communities from the rhizosphere and rhizoplane to bulk soil. Additionally, stochastic assembly processes drove the endosphere communities, whereas the soil, rhizosphere, and rhizoplane communities were governed primarily by the variable selection of deterministic processes, which showed increased importance from warm‐temperate to desert grasslands. Moreover, the properties of the microbial networks in the rhizoplane community indicate more stable networks in desert grasslands, likely conferring the resistance of microbial communities in higher stress environments. Collectively, our results showed that the bacterial communities in the soil‐root continuum had different sensitivities and assembly mechanisms along an environmental gradient. These patterns are shaped simultaneously by the intertwined dimensions of proximity to roots and environmental stress change in the Loess Plateau.

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Distinct and Temporally Stable Assembly Mechanisms Shape Bacterial and Fungal Communities in Vineyard Soils

et al. 2022

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Microbial communities in agricultural soils are fundamental for plant growth and in vineyard ecosystems contribute to defining regional wine quality. Managing soil microbes towards beneficial outcomes requires knowledge of how community assembly processes vary across taxonomic groups, spatial scales, and through time. However, our understanding of microbial assembly remains limited. To quantify the contributions of stochastic and deterministic processes to bacterial and fungal assembly across spatial scales and through time, we used 16 s rRNA gene and ITS sequencing in the soil of an emblematic wine-growing region of Italy.Combining null- and neutral-modelling, we found that assembly processes were consistent through time, but bacteria and fungi were governed by different processes. At the within-vineyard scale, deterministic selection and homogenising dispersal dominated bacterial assembly, while neither selection nor dispersal had clear influence over fungal assembly. At the among-vineyard scale, the influence of dispersal limitation increased for both taxonomic groups, but its contribution was much larger for fungal communities. These null-model-based inferences were supported by neutral modelling, which estimated a dispersal rate almost two orders-of-magnitude lower for fungi than bacteria.This indicates that while stochastic processes are important for fungal assembly, bacteria were more influenced by deterministic selection imposed by the biotic and/or abiotic environment. Managing microbes in vineyard soils could thus benefit from strategies that account for dispersal limitation of fungi and the importance of environmental conditions for bacteria. Our results are consistent with theoretical expectations whereby larger individual size and smaller populations can lead to higher levels of stochasticity.

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

Cited by 17 publications

References 85 publications

Advances in Defining Ecosystem Functions of the Terrestrial Subsurface Biosphere

Advances in Defining Ecosystem Functions of the Terrestrial Subsurface Biosphere

Differential microbial assembly processes and co‐occurrence networks in the soil‐root continuum along an environmental gradient

Distinct and Temporally Stable Assembly Mechanisms Shape Bacterial and Fungal Communities in Vineyard Soils

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