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      Shedding light on the composition of extreme microbial dark matter: alternative approaches for culturing extremophiles

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          Abstract

          More than 20,000 species of prokaryotes (less than 1% of the estimated number of Earth’s microbial species) have been described thus far. However, the vast majority of microbes that inhabit extreme environments remain uncultured and this group is termed “microbial dark matter.” Little is known regarding the ecological functions and biotechnological potential of these underexplored extremophiles, thus representing a vast untapped and uncharacterized biological resource. Advances in microbial cultivation approaches are key for a detailed and comprehensive characterization of the roles of these microbes in shaping the environment and, ultimately, for their biotechnological exploitation, such as for extremophile-derived bioproducts (extremozymes, secondary metabolites, CRISPR Cas systems, and pigments, among others), astrobiology, and space exploration. Additional efforts to enhance culturable diversity are required due to the challenges imposed by extreme culturing and plating conditions. In this review, we summarize methods and technologies used to recover the microbial diversity of extreme environments, while discussing the advantages and disadvantages associated with each of these approaches. Additionally, this review describes alternative culturing strategies to retrieve novel taxa with their unknown genes, metabolisms, and ecological roles, with the ultimate goal of increasing the yields of more efficient bio-based products. This review thus summarizes the strategies used to unveil the hidden diversity of the microbiome of extreme environments and discusses the directions for future studies of microbial dark matter and its potential applications in biotechnology and astrobiology.

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          Life in extreme environments.

          Each recent report of liquid water existing elsewhere in the Solar System has reverberated through the international press and excited the imagination of humankind. Why? Because in the past few decades we have come to realize that where there is liquid water on Earth, virtually no matter what the physical conditions, there is life. What we previously thought of as insurmountable physical and chemical barriers to life, we now see as yet another niche harbouring 'extremophiles'. This realization, coupled with new data on the survival of microbes in the space environment and modelling of the potential for transfer of life between celestial bodies, suggests that life could be more common than previously thought. Here we examine critically what it means to be an extremophile, and the implications of this for evolution, biotechnology and especially the search for life in the Universe.
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            A new view of the tree of life.

            The tree of life is one of the most important organizing principles in biology(1). Gene surveys suggest the existence of an enormous number of branches(2), but even an approximation of the full scale of the tree has remained elusive. Recent depictions of the tree of life have focused either on the nature of deep evolutionary relationships(3-5) or on the known, well-classified diversity of life with an emphasis on eukaryotes(6). These approaches overlook the dramatic change in our understanding of life's diversity resulting from genomic sampling of previously unexamined environments. New methods to generate genome sequences illuminate the identity of organisms and their metabolic capacities, placing them in community and ecosystem contexts(7,8). Here, we use new genomic data from over 1,000 uncultivated and little known organisms, together with published sequences, to infer a dramatically expanded version of the tree of life, with Bacteria, Archaea and Eukarya included. The depiction is both a global overview and a snapshot of the diversity within each major lineage. The results reveal the dominance of bacterial diversification and underline the importance of organisms lacking isolated representatives, with substantial evolution concentrated in a major radiation of such organisms. This tree highlights major lineages currently underrepresented in biogeochemical models and identifies radiations that are probably important for future evolutionary analyses.
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              Insights into the phylogeny and coding potential of microbial dark matter.

              Genome sequencing enhances our understanding of the biological world by providing blueprints for the evolutionary and functional diversity that shapes the biosphere. However, microbial genomes that are currently available are of limited phylogenetic breadth, owing to our historical inability to cultivate most microorganisms in the laboratory. We apply single-cell genomics to target and sequence 201 uncultivated archaeal and bacterial cells from nine diverse habitats belonging to 29 major mostly uncharted branches of the tree of life, so-called 'microbial dark matter'. With this additional genomic information, we are able to resolve many intra- and inter-phylum-level relationships and to propose two new superphyla. We uncover unexpected metabolic features that extend our understanding of biology and challenge established boundaries between the three domains of life. These include a novel amino acid use for the opal stop codon, an archaeal-type purine synthesis in Bacteria and complete sigma factors in Archaea similar to those in Bacteria. The single-cell genomes also served to phylogenetically anchor up to 20% of metagenomic reads in some habitats, facilitating organism-level interpretation of ecosystem function. This study greatly expands the genomic representation of the tree of life and provides a systematic step towards a better understanding of biological evolution on our planet.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                02 June 2023
                2023
                : 14
                : 1167718
                Affiliations
                [1] 1Red Sea Research Center, King Abdullah University of Science and Technology , Thuwal, Saudi Arabia
                [2] 2Computational Bioscience Research Center, King Abdullah University of Science and Technology , Thuwal, Saudi Arabia
                [3] 3Laboratory of Molecular Microbial Ecology, Institute of Microbiology, Federal University of Rio de Janeiro , Rio de Janeiro, Brazil
                Author notes

                Edited by: Andreas Teske, University of North Carolina at Chapel Hill, United States

                Reviewed by: Anirban Chakraborty, Idaho State University, United States; Melanie R. Mormile, Missouri University of Science and Technology, United States

                *Correspondence: Alexandre Soares Rosado, alexandre.rosado@ 123456kaust.edu.sa
                Article
                10.3389/fmicb.2023.1167718
                10272570
                37333658
                0c56e89d-df78-4dbd-9777-b45a1f43bce2
                Copyright © 2023 Schultz, Modolon, Peixoto and Rosado.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 16 February 2023
                : 09 May 2023
                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 215, Pages: 17, Words: 16509
                Funding
                Funded by: KAUST Baseline Grant
                Award ID: BAS/1/1096-01-01
                Funded by: National Council for Scientific and Technological Development, doi 10.13039/501100003593;
                Categories
                Microbiology
                Review
                Custom metadata
                Extreme Microbiology

                Microbiology & Virology
                extremophiles,extreme environments,microbial cultivation,applied microbiology,culturomics

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