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      The Rock-Hosted Biosphere

      1 , 1
      Annual Review of Earth and Planetary Sciences
      Annual Reviews

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          Abstract

          Our understanding of Earth's rock-hosted subsurface biosphere has advanced over the past two decades through the collection and analysis of fluids and rocks from aquifers within the continental and oceanic crust. Improvements in cell extraction, cell sorting, DNA sequencing, and techniques for detecting cell distributions and activity have revealed how the combination of lithology, permeability, and fluid mixing processes controls the diversity and heterogeneous distribution of microbial communities in fractured rock systems. However, the functions of most organisms, and the rates of their activity and growth, remain largely unknown. To mechanistically understand what physiochemical and hydrological factors control the rock-hosted biosphere, future studies are needed to characterize the physiology of microorganisms adapted to mineral-associated growth under energy- and nutrient-limited conditions. Experiments should be designed to detect synergistic interactions between microorganisms, and between microorganisms and minerals, at highly variable turnover rates.

          ▪ The heterogeneous distribution of the rock-hosted biosphere is controlled by variations in porosity, permeability, and chemical disequilibrium. ▪ Several imaging and chemical techniques can sensitively detect microbial activity within the rock-hosted biosphere. ▪ The physiology and turnover rates of the subsurface rock-hosted biosphere remain poorly known.

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          Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession.

          Ecological succession and the balance between stochastic and deterministic processes are two major themes within microbial ecology, but these conceptual domains have mostly developed independent of each other. Here we provide a framework that integrates shifts in community assembly processes with microbial primary succession to better understand mechanisms governing the stochastic/deterministic balance. Synthesizing previous work, we devised a conceptual model that links ecosystem development to alternative hypotheses related to shifts in ecological assembly processes. Conceptual model hypotheses were tested by coupling spatiotemporal data on soil bacterial communities with environmental conditions in a salt marsh chronosequence spanning 105 years of succession. Analyses within successional stages showed community composition to be initially governed by stochasticity, but as succession proceeded, there was a progressive increase in deterministic selection correlated with increasing sodium concentration. Analyses of community turnover among successional stages--which provide a larger spatiotemporal scale relative to within stage analyses--revealed that changes in the concentration of soil organic matter were the main predictor of the type and relative influence of determinism. Taken together, these results suggest scale-dependency in the mechanisms underlying selection. To better understand mechanisms governing these patterns, we developed an ecological simulation model that revealed how changes in selective environments cause shifts in the stochastic/deterministic balance. Finally, we propose an extended--and experimentally testable--conceptual model integrating ecological assembly processes with primary and secondary succession. This framework provides a priori hypotheses for future experiments, thereby facilitating a systematic approach to understand assembly and succession in microbial communities across ecosystems.
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            Extracellular electron transfer mechanisms between microorganisms and minerals.

            Electrons can be transferred from microorganisms to multivalent metal ions that are associated with minerals and vice versa. As the microbial cell envelope is neither physically permeable to minerals nor electrically conductive, microorganisms have evolved strategies to exchange electrons with extracellular minerals. In this Review, we discuss the molecular mechanisms that underlie the ability of microorganisms to exchange electrons, such as c-type cytochromes and microbial nanowires, with extracellular minerals and with microorganisms of the same or different species. Microorganisms that have extracellular electron transfer capability can be used for biotechnological applications, including bioremediation, biomining and the production of biofuels and nanomaterials.
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              Microbial life under extreme energy limitation.

              A great number of the bacteria and archaea on Earth are found in subsurface environments in a physiological state that is poorly represented or explained by laboratory cultures. Microbial cells in these very stable and oligotrophic settings catabolize 10⁴- to 10⁶-fold more slowly than model organisms in nutrient-rich cultures, turn over biomass on timescales of centuries to millennia rather than hours to days, and subsist with energy fluxes that are 1,000-fold lower than the typical culture-based estimates of maintenance requirements. To reconcile this disparate state of being with our knowledge of microbial physiology will require a revised understanding of microbial energy requirements, including identifying the factors that comprise true basal maintenance and the adaptations that might serve to minimize these factors.
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                Author and article information

                Journal
                Annual Review of Earth and Planetary Sciences
                Annu. Rev. Earth Planet. Sci.
                Annual Reviews
                0084-6597
                1545-4495
                May 31 2023
                May 31 2023
                : 51
                : 1
                : 493-519
                Affiliations
                [1 ]Department of Geological Sciences, University of Colorado, Boulder, Colorado, USA;
                Article
                10.1146/annurev-earth-031920-081957
                d53fd091-b528-4249-a453-5117a30b8edc
                © 2023

                http://creativecommons.org/licenses/by/4.0/

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