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      The Origin of Niches and Species in the Bacterial World

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          Abstract

          Niches are spaces for the biological units of selection, from cells to complex communities. In a broad sense, “species” are biological units of individuation. Niches do not exist without individual organisms, and every organism has a niche. We use “niche” in the Hutchinsonian sense as an abstraction of a multidimensional environmental space characterized by a variety of conditions, both biotic and abiotic, whose quantitative ranges determine the positive or negative growth rates of the microbial individual, typically a species, but also parts of the communities of species contained in this space. Microbial organisms (“species”) constantly diversify, and such diversification (radiation) depends on the possibility of opening up unexploited or insufficiently exploited niches. Niche exploitation frequently implies “niche construction,” as the colonized niche evolves with time, giving rise to new potential subniches, thereby influencing the selection of a series of new variants in the progeny. The evolution of niches and organisms is the result of reciprocal interacting processes that form a single unified process. Centrifugal microbial diversification expands the limits of the species’ niches while a centripetal or cohesive process occurs simultaneously, mediated by horizontal gene transfers and recombinatorial events, condensing all of the information recovered during the diversifying specialization into “novel organisms” (possible future species), thereby creating a more complex niche, where the selfishness of the new organism(s) establishes a “homeostatic power” limiting the niche’s variation. Once the niche’s full carrying capacity has been reached, reproductive isolation occurs, as no foreign organisms can outcompete the established population/community, thereby facilitating speciation. In the case of individualization-speciation of the microbiota, its contribution to the animal’ gut structure is a type of “niche construction,” the result of crosstalk between the niche (host) and microorganism(s). Lastly, there is a parallelism between the hierarchy of niches and that of microbial individuals. The increasing anthropogenic effects on the biosphere (such as globalization) might reduce the diversity of niches and bacterial individuals, with the potential emergence of highly transmissible multispecialists (which are eventually deleterious) resulting from the homogenization of the microbiosphere, a possibility that should be explored and prevented.

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          Most cited references126

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          High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries

          A fundamental question in microbiology is whether there is continuum of genetic diversity among genomes, or clear species boundaries prevail instead. Whole-genome similarity metrics such as Average Nucleotide Identity (ANI) help address this question by facilitating high resolution taxonomic analysis of thousands of genomes from diverse phylogenetic lineages. To scale to available genomes and beyond, we present FastANI, a new method to estimate ANI using alignment-free approximate sequence mapping. FastANI is accurate for both finished and draft genomes, and is up to three orders of magnitude faster compared to alignment-based approaches. We leverage FastANI to compute pairwise ANI values among all prokaryotic genomes available in the NCBI database. Our results reveal clear genetic discontinuity, with 99.8% of the total 8 billion genome pairs analyzed conforming to >95% intra-species and <83% inter-species ANI values. This discontinuity is manifested with or without the most frequently sequenced species, and is robust to historic additions in the genome databases.
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            The gut microbiota shapes intestinal immune responses during health and disease.

            Immunological dysregulation is the cause of many non-infectious human diseases such as autoimmunity, allergy and cancer. The gastrointestinal tract is the primary site of interaction between the host immune system and microorganisms, both symbiotic and pathogenic. In this Review we discuss findings indicating that developmental aspects of the adaptive immune system are influenced by bacterial colonization of the gut. We also highlight the molecular pathways that mediate host-symbiont interactions that regulate proper immune function. Finally, we present recent evidence to support that disturbances in the bacterial microbiota result in dysregulation of adaptive immune cells, and this may underlie disorders such as inflammatory bowel disease. This raises the possibility that the mammalian immune system, which seems to be designed to control microorganisms, is in fact controlled by microorganisms.
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              Evolution of mammals and their gut microbes.

              Mammals are metagenomic in that they are composed of not only their own gene complements but also those of all of their associated microbes. To understand the coevolution of the mammals and their indigenous microbial communities, we conducted a network-based analysis of bacterial 16S ribosomal RNA gene sequences from the fecal microbiota of humans and 59 other mammalian species living in two zoos and in the wild. The results indicate that host diet and phylogeny both influence bacterial diversity, which increases from carnivory to omnivory to herbivory; that bacterial communities codiversified with their hosts; and that the gut microbiota of humans living a modern life-style is typical of omnivorous primates.
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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
                17 March 2021
                2021
                : 12
                : 657986
                Affiliations
                [1] 1Division of Biology and Evolution of Microorganisms, Department of Microbiology, Ramón y Cajal Institute for Health Research (IRYCIS), Ramón y Cajal University Hospital , Madrid, Spain
                [2] 2National Center for Biotechnology (CNB-CSIC) , Madrid, Spain
                Author notes

                Edited by: Eric Daniel Becraft, University of North Alabama, United States

                Reviewed by: Mel Crystal Melendrez, Anoka-Ramsey Community College, United States; Valeria Souza, National Autonomous University of Mexico, Mexico

                *Correspondence: Fernando Baquero, baquero@ 123456bitmailer.net

                This article was submitted to Evolutionary and Genomic Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2021.657986
                8010147
                33815348
                f62231ee-e0aa-4184-b1ae-d8e81b8049fe
                Copyright © 2021 Baquero, Coque, Galán and Martinez.

                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
                : 24 January 2021
                : 23 February 2021
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 126, Pages: 13, Words: 0
                Funding
                Funded by: Joint Programming Initiative on Antimicrobial Resistance 10.13039/100013281
                Funded by: Ministerio de Ciencia, Innovación y Universidades 10.13039/100014440
                Funded by: Instituto de Salud Carlos III 10.13039/501100004587
                Categories
                Microbiology
                Review

                Microbiology & Virology
                bacterial niches,bacterial species,speciation,evolution,nichification
                Microbiology & Virology
                bacterial niches, bacterial species, speciation, evolution, nichification

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