Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers

ABSTRACT Sap-sucking hemipterans host specialized, heritable microorganisms that supplement their diet with essential nutrients. These microbes show unusual features that provide a unique perspective on the coevolution of host-symbiont systems but are still poorly understood. Here, we combine micros...

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Autores principales:	Anna Michalik, Diego Castillo Franco, Michał Kobiałka, Teresa Szklarzewicz, Adam Stroiński, Piotr Łukasik
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	planthoppers nutritional symbiosis transovarial transmission genomes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0e8a9e3e1b98416bb9cae2a4ff3c8016
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spelling	oai:doaj.org-article:0e8a9e3e1b98416bb9cae2a4ff3c80162021-11-10T18:37:51ZAlternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers10.1128/mBio.01228-212150-7511https://doaj.org/article/0e8a9e3e1b98416bb9cae2a4ff3c80162021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01228-21https://doaj.org/toc/2150-7511ABSTRACT Sap-sucking hemipterans host specialized, heritable microorganisms that supplement their diet with essential nutrients. These microbes show unusual features that provide a unique perspective on the coevolution of host-symbiont systems but are still poorly understood. Here, we combine microscopy with high-throughput sequencing to revisit 80-year-old reports on the diversity of symbiont transmission modes in a broadly distributed planthopper family, Dictyopharidae. We show that in seven species examined, the ancestral nutritional symbionts Sulcia and Vidania producing essential amino acids are complemented by co-primary symbionts, either Arsenophonus or Sodalis, acquired several times independently by different host lineages and contributing to the biosynthesis of B vitamins. These symbionts reside within separate bacteriomes within the abdominal cavity, although in females Vidania also occupies bacteriocytes in the rectal organ. Notably, the symbionts are transovarially transmitted from mothers to offspring in two alternative ways. In most examined species, all nutritional symbionts simultaneously infect the posterior end of the full-grown oocytes and next gather in their perivitelline space. In contrast, in other species, Sodalis colonizes the cytoplasm of the anterior pole of young oocytes, forming a cluster separate from the “symbiont ball” formed by late-invading Sulcia and Vidania. Our results show how newly arriving microbes may utilize different strategies to establish long-term heritable symbiosis. IMPORTANCE Sup-sucking hemipterans host ancient heritable microorganisms that supplement their unbalanced diet with essential nutrients and have repeatedly been complemented or replaced by other microorganisms. These symbionts need to be reliably transmitted to subsequent generations through the reproductive system, and often they end up using the same route as the most ancient ones. We show for the first time that in a single family of planthoppers, the complementing symbionts that have established infections independently utilize different transmission strategies, one of them novel, with the transmission of different microbes separated spatially and temporally. These data show how newly arriving microbes may utilize different strategies to establish long-term heritable symbioses.Anna MichalikDiego Castillo FrancoMichał KobiałkaTeresa SzklarzewiczAdam StroińskiPiotr ŁukasikAmerican Society for Microbiologyarticleplanthoppersnutritional symbiosistransovarial transmissiongenomesMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	planthoppers nutritional symbiosis transovarial transmission genomes Microbiology QR1-502
spellingShingle	planthoppers nutritional symbiosis transovarial transmission genomes Microbiology QR1-502 Anna Michalik Diego Castillo Franco Michał Kobiałka Teresa Szklarzewicz Adam Stroiński Piotr Łukasik Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers
description	ABSTRACT Sap-sucking hemipterans host specialized, heritable microorganisms that supplement their diet with essential nutrients. These microbes show unusual features that provide a unique perspective on the coevolution of host-symbiont systems but are still poorly understood. Here, we combine microscopy with high-throughput sequencing to revisit 80-year-old reports on the diversity of symbiont transmission modes in a broadly distributed planthopper family, Dictyopharidae. We show that in seven species examined, the ancestral nutritional symbionts Sulcia and Vidania producing essential amino acids are complemented by co-primary symbionts, either Arsenophonus or Sodalis, acquired several times independently by different host lineages and contributing to the biosynthesis of B vitamins. These symbionts reside within separate bacteriomes within the abdominal cavity, although in females Vidania also occupies bacteriocytes in the rectal organ. Notably, the symbionts are transovarially transmitted from mothers to offspring in two alternative ways. In most examined species, all nutritional symbionts simultaneously infect the posterior end of the full-grown oocytes and next gather in their perivitelline space. In contrast, in other species, Sodalis colonizes the cytoplasm of the anterior pole of young oocytes, forming a cluster separate from the “symbiont ball” formed by late-invading Sulcia and Vidania. Our results show how newly arriving microbes may utilize different strategies to establish long-term heritable symbiosis. IMPORTANCE Sup-sucking hemipterans host ancient heritable microorganisms that supplement their unbalanced diet with essential nutrients and have repeatedly been complemented or replaced by other microorganisms. These symbionts need to be reliably transmitted to subsequent generations through the reproductive system, and often they end up using the same route as the most ancient ones. We show for the first time that in a single family of planthoppers, the complementing symbionts that have established infections independently utilize different transmission strategies, one of them novel, with the transmission of different microbes separated spatially and temporally. These data show how newly arriving microbes may utilize different strategies to establish long-term heritable symbioses.
format	article
author	Anna Michalik Diego Castillo Franco Michał Kobiałka Teresa Szklarzewicz Adam Stroiński Piotr Łukasik
author_facet	Anna Michalik Diego Castillo Franco Michał Kobiałka Teresa Szklarzewicz Adam Stroiński Piotr Łukasik
author_sort	Anna Michalik
title	Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers
title_short	Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers
title_full	Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers
title_fullStr	Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers
title_full_unstemmed	Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers
title_sort	alternative transmission patterns in independently acquired nutritional cosymbionts of dictyopharidae planthoppers
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/0e8a9e3e1b98416bb9cae2a4ff3c8016
work_keys_str_mv	AT annamichalik alternativetransmissionpatternsinindependentlyacquirednutritionalcosymbiontsofdictyopharidaeplanthoppers AT diegocastillofranco alternativetransmissionpatternsinindependentlyacquirednutritionalcosymbiontsofdictyopharidaeplanthoppers AT michałkobiałka alternativetransmissionpatternsinindependentlyacquirednutritionalcosymbiontsofdictyopharidaeplanthoppers AT teresaszklarzewicz alternativetransmissionpatternsinindependentlyacquirednutritionalcosymbiontsofdictyopharidaeplanthoppers AT adamstroinski alternativetransmissionpatternsinindependentlyacquirednutritionalcosymbiontsofdictyopharidaeplanthoppers AT piotrłukasik alternativetransmissionpatternsinindependentlyacquirednutritionalcosymbiontsofdictyopharidaeplanthoppers
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Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers

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