The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology

ABSTRACT Mobile elements—plasmids and phages—are important components of microbial function and evolution via traits that they encode and their capacity to shuttle genetic material between species. We here report the unusually rich array of mobile elements within the genome of Arsenophonus nasoniae,...

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Autores principales:	Crystal L. Frost, Stefanos Siozios, Pol Nadal-Jimenez, Michael A. Brockhurst, Kayla C. King, Alistair C. Darby, Gregory D. D. Hurst
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	bacteriophage evolution endosymbionts genomics plasmids Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7626f462e08448c7b5952661fa697fc3
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spelling	oai:doaj.org-article:7626f462e08448c7b5952661fa697fc32021-11-15T15:57:03ZThe Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology10.1128/mBio.02590-192150-7511https://doaj.org/article/7626f462e08448c7b5952661fa697fc32020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02590-19https://doaj.org/toc/2150-7511ABSTRACT Mobile elements—plasmids and phages—are important components of microbial function and evolution via traits that they encode and their capacity to shuttle genetic material between species. We here report the unusually rich array of mobile elements within the genome of Arsenophonus nasoniae, the son-killer symbiont of the parasitic wasp Nasonia vitripennis. This microbe’s genome has the highest prophage complement reported to date, with over 50 genomic regions that represent either intact or degraded phage material. Moreover, the genome is predicted to include 17 extrachromosomal genetic elements, which carry many genes predicted to be important at the microbe-host interface, derived from a diverse assemblage of insect-associated gammaproteobacteria. In our system, this diversity was previously masked by repetitive mobile elements that broke the assembly derived from short reads. These findings suggest that other complex bacterial genomes will be revealed in the era of long-read sequencing. IMPORTANCE The biology of many bacteria is critically dependent on genes carried on plasmid and phage mobile elements. These elements shuttle between microbial species, thus providing an important source of biological innovation across taxa. It has recently been recognized that mobile elements are also important in symbiotic bacteria, which form long-lasting interactions with their host. In this study, we report a bacterial symbiont genome that carries a highly complex array of these elements. Arsenophonus nasoniae is the son-killer microbe of the parasitic wasp Nasonia vitripennis and exists with the wasp throughout its life cycle. We completed its genome with the aid of recently developed long-read technology. This assembly contained over 50 chromosomal regions of phage origin and 17 extrachromosomal elements within the genome, encoding many important traits at the host-microbe interface. Thus, the biology of this symbiont is enabled by a complex array of mobile elements.Crystal L. FrostStefanos SioziosPol Nadal-JimenezMichael A. BrockhurstKayla C. KingAlistair C. DarbyGregory D. D. HurstAmerican Society for Microbiologyarticlebacteriophage evolutionendosymbiontsgenomicsplasmidsMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacteriophage evolution endosymbionts genomics plasmids Microbiology QR1-502
spellingShingle	bacteriophage evolution endosymbionts genomics plasmids Microbiology QR1-502 Crystal L. Frost Stefanos Siozios Pol Nadal-Jimenez Michael A. Brockhurst Kayla C. King Alistair C. Darby Gregory D. D. Hurst The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology
description	ABSTRACT Mobile elements—plasmids and phages—are important components of microbial function and evolution via traits that they encode and their capacity to shuttle genetic material between species. We here report the unusually rich array of mobile elements within the genome of Arsenophonus nasoniae, the son-killer symbiont of the parasitic wasp Nasonia vitripennis. This microbe’s genome has the highest prophage complement reported to date, with over 50 genomic regions that represent either intact or degraded phage material. Moreover, the genome is predicted to include 17 extrachromosomal genetic elements, which carry many genes predicted to be important at the microbe-host interface, derived from a diverse assemblage of insect-associated gammaproteobacteria. In our system, this diversity was previously masked by repetitive mobile elements that broke the assembly derived from short reads. These findings suggest that other complex bacterial genomes will be revealed in the era of long-read sequencing. IMPORTANCE The biology of many bacteria is critically dependent on genes carried on plasmid and phage mobile elements. These elements shuttle between microbial species, thus providing an important source of biological innovation across taxa. It has recently been recognized that mobile elements are also important in symbiotic bacteria, which form long-lasting interactions with their host. In this study, we report a bacterial symbiont genome that carries a highly complex array of these elements. Arsenophonus nasoniae is the son-killer microbe of the parasitic wasp Nasonia vitripennis and exists with the wasp throughout its life cycle. We completed its genome with the aid of recently developed long-read technology. This assembly contained over 50 chromosomal regions of phage origin and 17 extrachromosomal elements within the genome, encoding many important traits at the host-microbe interface. Thus, the biology of this symbiont is enabled by a complex array of mobile elements.
format	article
author	Crystal L. Frost Stefanos Siozios Pol Nadal-Jimenez Michael A. Brockhurst Kayla C. King Alistair C. Darby Gregory D. D. Hurst
author_facet	Crystal L. Frost Stefanos Siozios Pol Nadal-Jimenez Michael A. Brockhurst Kayla C. King Alistair C. Darby Gregory D. D. Hurst
author_sort	Crystal L. Frost
title	The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology
title_short	The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology
title_full	The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology
title_fullStr	The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology
title_full_unstemmed	The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology
title_sort	hypercomplex genome of an insect reproductive parasite highlights the importance of lateral gene transfer in symbiont biology
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/7626f462e08448c7b5952661fa697fc3
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The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology

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