{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T10:21:00Z","timestamp":1790763660108,"version":"4.1.0"},"reference-count":75,"publisher":"The Royal Society","issue":"1983","license":[{"start":{"date-parts":[[2022,9,28]],"date-time":"2022-09-28T00:00:00Z","timestamp":1664323200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"funder":[{"DOI":"10.13039\/501100001711","name":"Swiss National Science Foundation","doi-asserted-by":"crossref","award":["P400PB_194337"],"award-info":[{"award-number":["P400PB_194337"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"crossref","award":["RGPAS-2020-00044"],"award-info":[{"award-number":["RGPAS-2020-00044"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"crossref","award":["RGPIN-2020-06996"],"award-info":[{"award-number":["RGPIN-2020-06996"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["royalsocietypublishing.org"],"crossmark-restriction":true},"short-container-title":["Proc. R. Soc. B."],"published-print":{"date-parts":[[2022,9,28]]},"abstract":"<jats:p>\n            <jats:italic>Wolbachia<\/jats:italic>\n            symbionts are the most successful host-associated microbes on the planet, infecting arthropods and nematodes. Their role in nematodes is particularly enigmatic, with filarial nematode species either 100% infected and dependent on symbionts for reproduction and development, or not at all infected. We have discovered a highly divergent strain of\n            <jats:italic>Wolbachia<\/jats:italic>\n            in an insect-parasitic tylenchid nematode,\n            <jats:italic>Howardula<\/jats:italic>\n            sp., in a nematode clade that has not previously been known to harbour\n            <jats:italic>Wolbachia<\/jats:italic>\n            . While this nematode is 100% infected with\n            <jats:italic>Wolbachia<\/jats:italic>\n            , we did not detect it in related species. We sequenced the\n            <jats:italic>Howardula<\/jats:italic>\n            symbiont (\n            <jats:italic>w<\/jats:italic>\n            How) genome and found that it is highly reduced, comprising only 550 kilobase pairs of DNA, approximately 35% smaller than the smallest\n            <jats:italic>Wolbachia<\/jats:italic>\n            nematode symbiont genomes. The\n            <jats:italic>w<\/jats:italic>\n            How genome is a subset of all other\n            <jats:italic>Wolbachia<\/jats:italic>\n            genomes and has not acquired any new genetic information. While it has lost many genes, including genes involved in cell wall synthesis and cell division, it has retained the entire haem biosynthesis pathway, suggesting that haem supplementation is critical.\n            <jats:italic>w<\/jats:italic>\n            How provides key insights into our understanding of what are the lower limits of\n            <jats:italic>Wolbachia<\/jats:italic>\n            cells, as well as the role of\n            <jats:italic>Wolbachia<\/jats:italic>\n            symbionts in the biology and convergent evolution of diverse parasitic nematodes.\n          <\/jats:p>","DOI":"10.1098\/rspb.2022.1518","type":"journal-article","created":{"date-parts":[[2022,9,28]],"date-time":"2022-09-28T07:06:01Z","timestamp":1664348761000},"update-policy":"https:\/\/doi.org\/10.1098\/crossmark-policy","source":"Crossref","is-referenced-by-count":19,"title":["A highly divergent\n            <i>Wolbachia<\/i>\n            with a tiny genome in an insect-parasitic tylenchid nematode"],"prefix":"10.1098","volume":"289","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1657-6958","authenticated-orcid":true,"given":"Jan P.","family":"Dudzic","sequence":"first","affiliation":[{"name":"Department of Biology, University of Victoria, Victoria, British Columbia, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8052-9670","authenticated-orcid":false,"given":"Caitlin I.","family":"Curtis","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Victoria, Victoria, British Columbia, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2461-9580","authenticated-orcid":false,"given":"Brent E.","family":"Gowen","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Victoria, Victoria, British Columbia, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9020-5506","authenticated-orcid":false,"given":"Steve J.","family":"Perlman","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Victoria, Victoria, British Columbia, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2022,9,28]]},"reference":[{"key":"e_1_3_6_2_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ento.42.1.587"},{"key":"e_1_3_6_3_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2021.03.006"},{"key":"e_1_3_6_4_2","doi-asserted-by":"publisher","DOI":"10.1186\/s13071-021-04742-1"},{"key":"e_1_3_6_5_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.devcel.2018.03.017"},{"key":"e_1_3_6_6_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature04756"},{"key":"e_1_3_6_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/bs.ctdb.2019.04.007"},{"key":"e_1_3_6_8_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.0030190"},{"key":"e_1_3_6_9_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0038544"},{"key":"e_1_3_6_10_2","doi-asserted-by":"publisher","DOI":"10.1111\/brv.12663"},{"key":"e_1_3_6_11_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1162418"},{"key":"e_1_3_6_12_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1000002"},{"key":"e_1_3_6_13_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.micro.53.1.71"},{"key":"e_1_3_6_14_2","first-page":"1","volume-title":"Influential passengers: inherited microorganisms and arthropod reproduction","author":"Werren JH","year":"1997","unstructured":"Werren JH, O'Neill SL. 1997 The evolution of heritable symbionts. In Influential passengers: inherited microorganisms and arthropod reproduction, pp. 1-41."},{"key":"e_1_3_6_15_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro1969"},{"key":"e_1_3_6_16_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2020.09.033"},{"key":"e_1_3_6_17_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature10356"},{"key":"e_1_3_6_18_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa2030243"},{"key":"e_1_3_6_19_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0911476107"},{"key":"e_1_3_6_20_2","doi-asserted-by":"publisher","DOI":"10.1128\/microbiolspec.BAI-0018-2019"},{"key":"e_1_3_6_21_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0065-308X(05)60004-8"},{"key":"e_1_3_6_22_2","doi-asserted-by":"publisher","DOI":"10.1007\/s13199-010-0067-1"},{"key":"e_1_3_6_23_2","doi-asserted-by":"publisher","DOI":"10.1111\/cmi.12084"},{"key":"e_1_3_6_24_2","doi-asserted-by":"publisher","DOI":"10.1101\/gr.138420.112"},{"key":"e_1_3_6_25_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.0030121"},{"key":"e_1_3_6_26_2","first-page":"e000487","article-title":"Diminutive, degraded but dissimilar: Wolbachia genomes from filarial nematodes do not conform to a single paradigm","volume":"6","author":"Lefoulon E","year":"2020","unstructured":"Lefoulon E et al. 2020 Diminutive, degraded but dissimilar: Wolbachia genomes from filarial nematodes do not conform to a single paradigm. Microb. Genom. 6, e000487. (doi:10.1099\/mgen.0.000487)","journal-title":"Microb. Genom."},{"key":"e_1_3_6_27_2","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-15-1041"},{"key":"e_1_3_6_28_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0000475"},{"key":"e_1_3_6_29_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijpara.2003.10.004"},{"key":"e_1_3_6_30_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0020843"},{"key":"e_1_3_6_31_2","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.1840"},{"key":"e_1_3_6_32_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijpara.2009.01.006"},{"key":"e_1_3_6_33_2","doi-asserted-by":"publisher","DOI":"10.1038\/srep34955"},{"key":"e_1_3_6_34_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2018.02482"},{"key":"e_1_3_6_35_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2019.00964"},{"key":"e_1_3_6_36_2","doi-asserted-by":"publisher","DOI":"10.1155\/2014\/135218"},{"key":"e_1_3_6_37_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ympev.2007.02.027"},{"key":"e_1_3_6_38_2","first-page":"1","article-title":"A revision of the genus Spelobia Spuler (Diptera: Sphaeroceridae) in North America and Mexico","volume":"111","author":"Marshall SA","year":"1985","unstructured":"Marshall SA. 1985 A revision of the genus Spelobia Spuler (Diptera: Sphaeroceridae) in North America and Mexico. Trans. Am. Entomol. Soc. 111, 1-101.","journal-title":"Trans. Am. Entomol. Soc."},{"key":"e_1_3_6_39_2","doi-asserted-by":"publisher","DOI":"10.1111\/mmi.13880"},{"key":"e_1_3_6_40_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro2670"},{"key":"e_1_3_6_41_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00731-06"},{"key":"e_1_3_6_42_2","doi-asserted-by":"publisher","DOI":"10.1017\/S003118200002672X"},{"issue":"45","key":"e_1_3_6_43_2","article-title":"The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics","volume":"1","author":"Stein LD","year":"2003","unstructured":"Stein LD et al. 2003 The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLOS Biology 1, e45. (doi:10.1371\/journal.pbio.0000045)","journal-title":"PLOS Biology"},{"key":"e_1_3_6_44_2","doi-asserted-by":"publisher","DOI":"10.1186\/1756-3305-4-228"},{"key":"e_1_3_6_45_2","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.15715"},{"key":"e_1_3_6_46_2","doi-asserted-by":"publisher","DOI":"10.1038\/ismej.2015.119"},{"key":"e_1_3_6_47_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-294X.2003.01721.x"},{"key":"e_1_3_6_48_2","unstructured":"Sims K. 2010 Interactions between Frankliniella fusca (Thysanoptera: Thripidae) Thripinema fuscum (Tylenchida: Allantonematidae) and entomoparasites (tomato spotted wilt virus Pantoea ananatis and Wolbachia ). PhD thesis University of Florida Gainesville FL USA."},{"key":"e_1_3_6_49_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tim.2017.02.014"},{"key":"e_1_3_6_50_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2000860117"},{"key":"e_1_3_6_51_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41396-021-01102-w"},{"key":"e_1_3_6_52_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41396-021-01056-z"},{"key":"e_1_3_6_53_2","doi-asserted-by":"publisher","DOI":"10.1038\/214174a0"},{"key":"e_1_3_6_54_2","doi-asserted-by":"publisher","DOI":"10.11646\/zootaxa.2633.1.1"},{"key":"e_1_3_6_55_2","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1079\/9780851992020.0000","volume-title":"Tylenchida: parasites of plants and insects","author":"Siddiqi MR","year":"2000","unstructured":"Siddiqi MR. 2000 Tylenchida: parasites of plants and insects, 833 p, 2nd edn. Wallingford, UK; New York, NY: CABI Publishing.","edition":"2"},{"key":"e_1_3_6_56_2","article-title":"Extremely reduced supergroup F Wolbachia\u202f: transition to obligate insect symbionts","author":"Mahmood S","year":"2021","unstructured":"Mahmood S, Nov\u00e1kov\u00e1 E, Martin\u016f J, Sychra O, Hyp\u0161a V. 2021 Extremely reduced supergroup F Wolbachia\u202f: transition to obligate insect symbionts. bioRxiv (cited 7 June 2022). (doi:10.1101\/2021.10.15.464041)","journal-title":"bioRxiv"},{"key":"e_1_3_6_57_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.genet.41.110306.130119"},{"key":"e_1_3_6_58_2","doi-asserted-by":"publisher","DOI":"10.1093\/gbe\/evv108"},{"key":"e_1_3_6_59_2","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.01342-21"},{"key":"e_1_3_6_60_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijmm.2013.01.002"},{"key":"e_1_3_6_61_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2019.08.054"},{"key":"e_1_3_6_62_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M901528200"},{"key":"e_1_3_6_63_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0003096"},{"key":"e_1_3_6_64_2","doi-asserted-by":"publisher","DOI":"10.1038\/ng.2585"},{"key":"e_1_3_6_65_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0500877102"},{"key":"e_1_3_6_66_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0058458"},{"key":"e_1_3_6_67_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1304049110"},{"key":"e_1_3_6_68_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2120003119"},{"key":"e_1_3_6_69_2","doi-asserted-by":"publisher","DOI":"10.1086\/342137"},{"key":"e_1_3_6_70_2","doi-asserted-by":"publisher","DOI":"10.1093\/jee\/77.2.449"},{"key":"e_1_3_6_71_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2000.1139"},{"key":"e_1_3_6_72_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.180.9.2373-2378.1998"},{"key":"e_1_3_6_73_2","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.2089"},{"key":"e_1_3_6_74_2","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1007\/978-1-349-09857-6","volume-title":"Principles and techniques of electron microscopy: biological applications","author":"Hayat MA","year":"1989","unstructured":"Hayat MA. 1989 Principles and techniques of electron microscopy: biological applications, 469 p, 3rd edn. Boca Raton, FL: CRC Press.","edition":"3"},{"key":"e_1_3_6_75_2","doi-asserted-by":"crossref","unstructured":"Dudzic JP Curtis CI Gowen BE Perlman SJ. 2022 Data from: A highly divergent Wolbachia with a tiny genome in an insect-parasitic tylenchid nematode. Dryad Digital Repository. (doi:10.5061\/dryad.98sf7m0ms)","DOI":"10.1098\/rspb.2022.1518"},{"key":"e_1_3_6_76_2","doi-asserted-by":"crossref","unstructured":"Dudzic JP Curtis CI Gowen BE Perlman SJ. 2022 A highly divergent Wolbachia with a tiny genome in an insect-parasitic tylenchid nematode. Figshare. (doi:10.6084\/m9.figshare.c.6189550)","DOI":"10.1098\/rspb.2022.1518"}],"container-title":["Proceedings of the Royal Society B: Biological Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2022.1518","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/full-xml\/10.1098\/rspb.2022.1518","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2022.1518","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,24]],"date-time":"2023-04-24T09:21:54Z","timestamp":1682328114000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/doi\/10.1098\/rspb.2022.1518"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,28]]},"references-count":75,"journal-issue":{"issue":"1983","published-print":{"date-parts":[[2022,9,28]]}},"alternative-id":["10.1098\/rspb.2022.1518"],"URL":"https:\/\/doi.org\/10.1098\/rspb.2022.1518","relation":{},"ISSN":["0962-8452","1471-2954"],"issn-type":[{"value":"0962-8452","type":"print"},{"value":"1471-2954","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,28]]},"assertion":[{"value":"2022-08-03","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-08-31","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-09-28","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"20221518"}}