A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosus
ABSTRACT Free-living bacteria have evolved multiple times to become host-restricted endosymbionts. The transition from a free-living to a host-restricted lifestyle comes with a number of different genomic changes, including a massive loss of genes. In host-restricted endosymbionts, gene inactivation...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02627-22 |
| _version_ | 1811290065470488576 |
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| author | Tamara Halter Frederik Hendrickx Matthias Horn Alejandro Manzano-Marín |
| author_facet | Tamara Halter Frederik Hendrickx Matthias Horn Alejandro Manzano-Marín |
| author_sort | Tamara Halter |
| collection | DOAJ |
| description | ABSTRACT Free-living bacteria have evolved multiple times to become host-restricted endosymbionts. The transition from a free-living to a host-restricted lifestyle comes with a number of different genomic changes, including a massive loss of genes. In host-restricted endosymbionts, gene inactivation and genome reduction are facilitated by mobile genetic elements, mainly insertion sequences (ISs). ISs are small autonomous mobile elements, and one of, if not the most, abundant transposable elements in bacteria. Proliferation of ISs is common in some facultative endosymbionts, and is likely driven by the transmission bottlenecks, which increase the level of genetic drift. In this study, we present a manually curated genome annotation for a Cardinium endosymbiont of the dwarf spider Oedothorax gibbosus. Cardinium species are host-restricted endosymbionts that, similarly to ColbachiaWolbachia spp., include strains capable of manipulating host reproduction. Through the focus on mobile elements, the annotation revealed a rampant spread of ISs, extending earlier observations in other Cardinium genomes. We found that a large proportion of IS elements are pseudogenized, with many displaying evidence of recent inactivation. Most notably, we describe the lineage-specific emergence and spread of a novel IS-derived Miniature Inverted repeat Transposable Element (MITE), likely being actively maintained by intact copies of its parental IS982-family element. This study highlights the relevance of manual curation of these repeat-rich endosymbiont genomes for the discovery of novel MITEs, as well as the possible role these understudied elements might play in genome streamlining. IMPORTANCE Cardinium bacteria, a widespread symbiont lineage found across insects and nematodes, have been linked to reproductive manipulation of their hosts. However, the study of Cardinium has been hampered by the lack of comprehensive genomic resources. The high content of mobile genetic elements, namely, insertion sequences (ISs), has long complicated the analyses and proper annotations of these genomes. In this study, we present a manually curated annotation of the Cardinium symbiont of the spider Oedothorax gibbosus. Most notably, we describe a novel IS-like element found exclusively in this strain. We show that this mobile element likely evolved from a defective copy of its parental IS and then spread throughout the genome, contributing to the pseudogenization of several other mobile elements. We propose this element is likely being maintained by the intact copies of its parental IS element and that other similar elements in the genome could potentially follow this route. |
| first_indexed | 2024-04-13T04:06:23Z |
| format | Article |
| id | doaj.art-29bd0665dc0c4c7896f8308720482c51 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-13T04:06:23Z |
| publishDate | 2022-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-29bd0665dc0c4c7896f8308720482c512022-12-22T03:03:14ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-12-0110610.1128/spectrum.02627-22A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosusTamara Halter0Frederik Hendrickx1Matthias Horn2Alejandro Manzano-Marín3Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, AustriaOD Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Brussels, BelgiumCentre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, AustriaCentre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, AustriaABSTRACT Free-living bacteria have evolved multiple times to become host-restricted endosymbionts. The transition from a free-living to a host-restricted lifestyle comes with a number of different genomic changes, including a massive loss of genes. In host-restricted endosymbionts, gene inactivation and genome reduction are facilitated by mobile genetic elements, mainly insertion sequences (ISs). ISs are small autonomous mobile elements, and one of, if not the most, abundant transposable elements in bacteria. Proliferation of ISs is common in some facultative endosymbionts, and is likely driven by the transmission bottlenecks, which increase the level of genetic drift. In this study, we present a manually curated genome annotation for a Cardinium endosymbiont of the dwarf spider Oedothorax gibbosus. Cardinium species are host-restricted endosymbionts that, similarly to ColbachiaWolbachia spp., include strains capable of manipulating host reproduction. Through the focus on mobile elements, the annotation revealed a rampant spread of ISs, extending earlier observations in other Cardinium genomes. We found that a large proportion of IS elements are pseudogenized, with many displaying evidence of recent inactivation. Most notably, we describe the lineage-specific emergence and spread of a novel IS-derived Miniature Inverted repeat Transposable Element (MITE), likely being actively maintained by intact copies of its parental IS982-family element. This study highlights the relevance of manual curation of these repeat-rich endosymbiont genomes for the discovery of novel MITEs, as well as the possible role these understudied elements might play in genome streamlining. IMPORTANCE Cardinium bacteria, a widespread symbiont lineage found across insects and nematodes, have been linked to reproductive manipulation of their hosts. However, the study of Cardinium has been hampered by the lack of comprehensive genomic resources. The high content of mobile genetic elements, namely, insertion sequences (ISs), has long complicated the analyses and proper annotations of these genomes. In this study, we present a manually curated annotation of the Cardinium symbiont of the spider Oedothorax gibbosus. Most notably, we describe a novel IS-like element found exclusively in this strain. We show that this mobile element likely evolved from a defective copy of its parental IS and then spread throughout the genome, contributing to the pseudogenization of several other mobile elements. We propose this element is likely being maintained by the intact copies of its parental IS element and that other similar elements in the genome could potentially follow this route.https://journals.asm.org/doi/10.1128/spectrum.02627-22Cardiniummobile elementinsertion sequenceendosymbiontAmoebophilaceae |
| spellingShingle | Tamara Halter Frederik Hendrickx Matthias Horn Alejandro Manzano-Marín A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosus Microbiology Spectrum Cardinium mobile element insertion sequence endosymbiont Amoebophilaceae |
| title | A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosus |
| title_full | A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosus |
| title_fullStr | A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosus |
| title_full_unstemmed | A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosus |
| title_short | A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosus |
| title_sort | novel widespread mite element in the repeat rich genome of the cardinium endosymbiont of the spider oedothorax gibbosus |
| topic | Cardinium mobile element insertion sequence endosymbiont Amoebophilaceae |
| url | https://journals.asm.org/doi/10.1128/spectrum.02627-22 |
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