{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T13:57:52Z","timestamp":1790344672938,"version":"4.1.0"},"reference-count":36,"publisher":"American Society for Microbiology","issue":"7","license":[{"start":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T00:00:00Z","timestamp":1783468800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T00:00:00Z","timestamp":1783468800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"DOI":"10.13039\/501100002241","name":"Japan Science and Technology Agency","doi-asserted-by":"publisher","award":["JPMJER1902"],"award-info":[{"award-number":["JPMJER1902"]}],"id":[{"id":"10.13039\/501100002241","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002241","name":"Japan Science and Technology Agency","doi-asserted-by":"publisher","award":["JPMJCR25B4"],"award-info":[{"award-number":["JPMJCR25B4"]}],"id":[{"id":"10.13039\/501100002241","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP24H02298"],"award-info":[{"award-number":["JP24H02298"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["mBio"],"published-print":{"date-parts":[[2026,7,8]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:sec>\n                    <jats:title\/>\n                    <jats:p>\n                      The stinkbug\n                      <jats:italic toggle=\"yes\">Plautia stali<\/jats:italic>\n                      harbors essential gut symbiotic bacteria of the genus\n                      <jats:italic toggle=\"yes\">Pantoea<\/jats:italic>\n                      , whose natural strains differ in cultivability and host benefits. Using this system, we evaluated how laboratory-evolved and genetically engineered symbiotic\n                      <jats:italic toggle=\"yes\">Escherichia coli<\/jats:italic>\n                      strains compete against native\n                      <jats:italic toggle=\"yes\">Pantoea<\/jats:italic>\n                      symbionts and how they influence host fitness. In single infection assays, the native uncultivable symbiont Sym A conferred the highest host performance, whereas the evolved (CmL05G13) and artificial (\u0394\n                      <jats:italic toggle=\"yes\">cyaA<\/jats:italic>\n                      ) symbiotic\n                      <jats:italic toggle=\"yes\">E. coli<\/jats:italic>\n                      strains supported host survival at levels comparable to cultivable\n                      <jats:italic toggle=\"yes\">Pantoea<\/jats:italic>\n                      symbionts (Sym C\u2013F). In competitive co-infection assays, the symbiotic\n                      <jats:italic toggle=\"yes\">E. coli<\/jats:italic>\n                      strains generally showed unexpectedly strong colonization ability. CmL05G13 outcompeted all the cultivable symbionts Sym C\u2013F and even displaced the native uncultivable symbiont Sym A, whereas \u0394\n                      <jats:italic toggle=\"yes\">cyaA<\/jats:italic>\n                      and the nonsymbiotic control\n                      <jats:italic toggle=\"yes\">E. coli<\/jats:italic>\n                      \u0394\n                      <jats:italic toggle=\"yes\">intS<\/jats:italic>\n                      were dominated by Sym A at the adult stage. Despite their superior infection competitiveness, the symbiotic\n                      <jats:italic toggle=\"yes\">E. coli<\/jats:italic>\n                      strains provided limited reproductive benefits, behaving as \u201ccheater-like\u201d associates. They were able to invade and dominate the symbiotic organ but failed to match the fitness contributions of native symbionts. These results demonstrate that the experimentally evolved\n                      <jats:italic toggle=\"yes\">E. coli<\/jats:italic>\n                      can rapidly acquire strong colonization ability, surpassing that of the natural symbionts that have coevolved with\n                      <jats:italic toggle=\"yes\">P. stali<\/jats:italic>\n                      in nature. At the same time, the mismatch between infection success and host fitness benefits highlights potential evolutionary conflicts and provides an experimental model for studying the dynamics of cheating, mutualism, and symbiont replacement in vertically transmitted symbioses.\n                    <\/jats:p>\n                    <jats:sec>\n                      <jats:title>IMPORTANCE<\/jats:title>\n                      <jats:p>\n                        Understanding how novel symbionts invade and displace long-term mutualists is central to the evolution of symbiosis. This study demonstrates that\n                        <jats:italic toggle=\"yes\">Escherichia coli<\/jats:italic>\n                        , originally a nonsymbiotic bacterium, can rapidly evolve potent colonization ability and even outcompete native\n                        <jats:italic toggle=\"yes\">Pantoea<\/jats:italic>\n                        symbionts of the stinkbug\n                        <jats:italic toggle=\"yes\">Plautia stali<\/jats:italic>\n                        . Meanwhile, these competitive\n                        <jats:italic toggle=\"yes\">E. coli<\/jats:italic>\n                        strains confer markedly lower reproductive benefits compared with the native symbionts that have developed an intimate mutualistic association with the host\n                        <jats:italic toggle=\"yes\">P. stali<\/jats:italic>\n                        over evolutionary time, revealing a striking decoupling between infection success and host fitness. This finding highlights the potential for cheater-like microbes to invade vertically transmitted symbioses and destabilize coevolved partnerships. By combining experimental evolution, controlled co-infections, and quantitative analyses, the\n                        <jats:italic toggle=\"yes\">P. stali-E. coli<\/jats:italic>\n                        experimental symbiotic system provides a powerful model for studying the mechanisms and evolutionary dynamics of mutualism, cheating, and symbiont replacement.\n                      <\/jats:p>\n                    <\/jats:sec>\n                  <\/jats:sec>","DOI":"10.1128\/mbio.00951-26","type":"journal-article","created":{"date-parts":[[2026,6,15]],"date-time":"2026-06-15T13:00:54Z","timestamp":1781528454000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":2,"title":["Symbiotic\n                    <i>Escherichia coli<\/i>\n                    strains can better colonize host stinkbugs and outcompete natural symbiotic bacteria, but confer less fitness benefit"],"prefix":"10.1128","volume":"17","author":[{"given":"Wenjin","family":"Cai","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01703db54","id-type":"ROR","asserted-by":"publisher"}],"name":"Molecular Biosystems Research Institute, National Institute of Advanced Industrial Science and Technology (AIST)","place":["Tsukuba, Japan"]},{"id":[{"id":"https:\/\/ror.org\/057zh3y96","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biological Sciences, Graduate School of Science, The University of Tokyo","place":["Tokyo, Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4369-6477","authenticated-orcid":true,"given":"Minoru","family":"Moriyama","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01703db54","id-type":"ROR","asserted-by":"publisher"}],"name":"Molecular Biosystems Research Institute, National Institute of Advanced Industrial Science and Technology (AIST)","place":["Tsukuba, Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yudai","family":"Nishide","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/023v4bd62","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Agrobiological Sciences Ohwashi, National Agriculture and Food Research Organization (NARO)","place":["Tsukuba, Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryuichi","family":"Koga","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01703db54","id-type":"ROR","asserted-by":"publisher"}],"name":"Molecular Biosystems Research Institute, National Institute of Advanced Industrial Science and Technology (AIST)","place":["Tsukuba, Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5987-2602","authenticated-orcid":true,"given":"Takema","family":"Fukatsu","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01703db54","id-type":"ROR","asserted-by":"publisher"}],"name":"Molecular Biosystems Research Institute, National Institute of Advanced Industrial Science and Technology (AIST)","place":["Tsukuba, Japan"]},{"id":[{"id":"https:\/\/ror.org\/057zh3y96","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biological Sciences, Graduate School of Science, The University of Tokyo","place":["Tokyo, Japan"]},{"id":[{"id":"https:\/\/ror.org\/02956yf07","id-type":"ROR","asserted-by":"publisher"}],"name":"Graduate School of Life and Environmental Sciences, University of Tsukuba","place":["Tsukuba, Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_5_2_2","volume-title":"Endosymbiosis of animals with plant microorganisms","author":"Buchner P","year":"1965","unstructured":"Buchner P. 1965. Endosymbiosis of animals with plant microorganisms. Interscience Publishers."},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1218525110"},{"key":"e_1_3_5_4_2","volume-title":"Insects and their beneficial microbes","author":"Douglas AE","year":"2022","unstructured":"Douglas AE. 2022. Insects and their beneficial microbes. Princeton University Press."},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.01444"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41579-021-00550-7"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1186\/s40851-019-0134-2"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1128\/mbio.00522-23"},{"key":"e_1_3_5_9_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00114-025-01986-0"},{"key":"e_1_3_5_10_2","doi-asserted-by":"publisher","DOI":"10.1038\/nmicrobiol.2015.11"},{"key":"e_1_3_5_11_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-022-11895-1"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1007\/s13355-025-00897-w"},{"key":"e_1_3_5_13_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41564-022-01179-9"},{"key":"e_1_3_5_14_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41564-026-02264-z"},{"key":"e_1_3_5_15_2","doi-asserted-by":"publisher","DOI":"10.1128\/mbio.03883-25"},{"key":"e_1_3_5_16_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tim.2016.06.011"},{"key":"e_1_3_5_17_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro2259"},{"key":"e_1_3_5_18_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1912397116"},{"key":"e_1_3_5_19_2","doi-asserted-by":"publisher","DOI":"10.1093\/ismejo\/wraf240"},{"key":"e_1_3_5_20_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.3002304"},{"key":"e_1_3_5_21_2","doi-asserted-by":"publisher","DOI":"10.1007\/s13355-017-0495-y"},{"key":"e_1_3_5_22_2","doi-asserted-by":"publisher","DOI":"10.1128\/mbio.01342-24"},{"key":"e_1_3_5_23_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41564-022-01188-8"},{"key":"e_1_3_5_24_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2001.1900"},{"key":"e_1_3_5_25_2","doi-asserted-by":"publisher","DOI":"10.1086\/673757"},{"key":"e_1_3_5_26_2","doi-asserted-by":"publisher","DOI":"10.1111\/ele.12507"},{"key":"e_1_3_5_27_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2023.06.081"},{"key":"e_1_3_5_28_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.04057-14"},{"key":"e_1_3_5_29_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00067-07"},{"key":"e_1_3_5_30_2","doi-asserted-by":"publisher","DOI":"10.1264\/jsme2.ME19011"},{"key":"e_1_3_5_31_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2021.719112"},{"key":"e_1_3_5_32_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1511454112"},{"key":"e_1_3_5_33_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2401802121"},{"key":"e_1_3_5_34_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02152-13"},{"key":"e_1_3_5_35_2","doi-asserted-by":"publisher","DOI":"10.1007\/s13355-024-00874-9"},{"key":"e_1_3_5_36_2","doi-asserted-by":"publisher","DOI":"10.1038\/msb4100050"},{"key":"e_1_3_5_37_2","doi-asserted-by":"publisher","DOI":"10.2144\/00291bm09"}],"container-title":["mBio"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mbio.00951-26","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mbio.00951-26","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T13:02:19Z","timestamp":1783515739000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/mbio.00951-26"}},"subtitle":[],"editor":[{"given":"Marvin","family":"Whiteley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,7,8]]},"references-count":36,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2026,7,8]]}},"alternative-id":["10.1128\/mbio.00951-26"],"URL":"https:\/\/doi.org\/10.1128\/mbio.00951-26","relation":{},"ISSN":["2150-7511"],"issn-type":[{"value":"2150-7511","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,8]]},"assertion":[{"value":"2026-04-22","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-05-10","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-06-15","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e00951-26"}}