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Endomicrobia, a family-level lineage of host-associated bacteria in the phylum\n                      <jats:italic>Elusimicrobiota<\/jats:italic>\n                      that comprises both free-living representatives and endosymbionts of termite gut flagellates, are an excellent model to study evolution of intracellular symbionts. We reconstructed 67 metagenome-assembled genomes (MAGs) of\n                      <jats:italic>Endomicrobiaceae<\/jats:italic>\n                      among more than 1,700 MAGs from the gut microbiota of a wide range of termites. Phylogenomic analysis confirmed a sister position of representatives from termites and ruminants, and allowed to propose eight new genera in the radiation of\n                      <jats:italic>Endomicrobiaceae<\/jats:italic>\n                      . Comparative genome analysis documented progressive genome erosion in the new genus\n                      <jats:italic>Endomicrobiellum<\/jats:italic>\n                      , which comprises all flagellate endosymbionts characterized to date. Massive gene losses were accompanied by the acquisition of new functions by horizontal gene transfer, which led to a shift from a glucose-based energy metabolism to one based on sugar phosphates. The breakdown of glycolysis and many anabolic pathways for amino acids and cofactors in several subgroups was compensated by the independent acquisition of new uptake systems, including an ATP\/ADP antiporter, from other gut microbiota. The putative donors are mostly flagellate endosymbionts from other bacterial phyla, including several, hitherto unknown lineages of uncultured\n                      <jats:italic>Alphaproteobacteria<\/jats:italic>\n                      , documenting the importance of horizontal gene transfer in the convergent evolution of these intracellular symbioses. The loss of almost all biosynthetic capacities in some lineages of\n                      <jats:italic>Endomicrobiellum<\/jats:italic>\n                      suggests that their originally mutualistic relationship with flagellates is on its decline.\n                    <\/jats:p>\n                    <jats:sec>\n                      <jats:title>IMPORTANCE<\/jats:title>\n                      <jats:p>Unicellular eukaryotes are frequently colonized by bacterial and archaeal symbionts. A prominent example are the cellulolytic gut flagellates of termites, which harbor diverse but host-specific bacterial symbionts that occur exclusively in termite guts. One of these lineages, the so-called Endomicrobia, comprises both free-living and endosymbiotic representatives, which offers the unique opportunity to study the evolutionary processes underpinning the transition from a free-living to an intracellular lifestyle. Our results revealed a progressive gene loss in energy metabolism and biosynthetic pathways, compensated by the acquisition of new functions via horizontal gene transfer from other gut bacteria, and suggest the eventual breakdown of an initially mutualistic symbiosis. Evidence for convergent evolution of unrelated endosymbionts reflects adaptations to the intracellular environment of termite gut flagellates.<\/jats:p>\n                    <\/jats:sec>\n                  <\/jats:sec>","DOI":"10.1128\/mbio.00826-24","type":"journal-article","created":{"date-parts":[[2024,5,14]],"date-time":"2024-05-14T09:01:07Z","timestamp":1715677267000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":20,"title":["Genome reduction and horizontal gene transfer in the evolution of Endomicrobia\u2014rise and fall of an intracellular symbiosis with termite gut flagellates"],"prefix":"10.1128","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4879-7325","authenticated-orcid":true,"given":"Undine S.","family":"Mies","sequence":"first","affiliation":[{"name":"Research Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3495-561X","authenticated-orcid":false,"given":"Vincent","family":"Herv\u00e9","sequence":"additional","affiliation":[{"name":"Research Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tom","family":"Kropp","sequence":"additional","affiliation":[{"name":"Research Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5093-6155","authenticated-orcid":false,"given":"Katja","family":"Platt","sequence":"additional","affiliation":[{"name":"Research Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5027-8703","authenticated-orcid":false,"given":"David","family":"Sillam-Duss\u00e8s","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental and Comparative Ethology LEEC, UR 4443, University Sorbonne Paris Nord, Villetaneuse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8581-637X","authenticated-orcid":true,"given":"Jan","family":"\u0160obotn\u00edk","sequence":"additional","affiliation":[{"name":"Faculty of Tropical AgriSciences, Czech University of Life Sciences, Prague, Czechia"},{"name":"Biology Centre, Czech Academy of Sciences, Institute of Entomology, \u010cesk\u00e9 Bud\u011bjovice, Czechia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2667-4391","authenticated-orcid":true,"given":"Andreas","family":"Brune","sequence":"additional","affiliation":[{"name":"Research Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_5_2_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro2670"},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.1111\/nyas.12740"},{"key":"e_1_3_5_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2019.12.070"},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2021.05.049"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.71.3.1473-1479.2005"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.2007\/009217-0"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6941.2007.00311.x"},{"key":"e_1_3_5_9_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.00961"},{"key":"e_1_3_5_10_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2018.02526"},{"key":"e_1_3_5_11_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1758-2229.2009.00124.x"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1111\/1758-2229.12565"},{"key":"e_1_3_5_13_2","first-page":"413","volume-title":"Biology of termites: a modern synthesis","author":"Ohkuma M","year":"2011","unstructured":"Ohkuma M, Brune A. 2011. 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