Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions

Infectious disease outbreaks are causing widespread declines of marine invertebrates including corals, sea stars, shrimps, and molluscs. Dermo is a lethal infectious disease of the eastern oyster Crassostrea virginica caused by the protist Perkinsus marinus. The Pacific oyster Crassostrea gigas is r...

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Autores principales:	Jiulin Chan, Lu Wang, Li Li, Kang Mu, David Bushek, Yue Xu, Ximing Guo, Guofan Zhang, Linlin Zhang
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	oyster comparative transcriptomics dermo disease innate immune response host-parasite interaction Genetics QH426-470
Acceso en línea:	https://doaj.org/article/886e83fd6d514cfa82756eaf24e82f9e
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spelling	oai:doaj.org-article:886e83fd6d514cfa82756eaf24e82f9e2021-12-03T06:27:43ZTranscriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions1664-802110.3389/fgene.2021.795706https://doaj.org/article/886e83fd6d514cfa82756eaf24e82f9e2021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fgene.2021.795706/fullhttps://doaj.org/toc/1664-8021Infectious disease outbreaks are causing widespread declines of marine invertebrates including corals, sea stars, shrimps, and molluscs. Dermo is a lethal infectious disease of the eastern oyster Crassostrea virginica caused by the protist Perkinsus marinus. The Pacific oyster Crassostrea gigas is resistant to Dermo due to differences in the host-parasite interaction that is not well understood. We compared transcriptomic responses to P. marinus challenge in the two oysters at early and late infection stages. Dynamic and orchestrated regulation of large sets of innate immune response genes were observed in both species with remarkably similar patterns for most orthologs, although responses in C. virginica were stronger, suggesting strong or over-reacting immune response could be a cause of host mortality. Between the two species, several key immune response gene families differed in their expansion, sequence variation and/or transcriptional response to P. marinus, reflecting evolutionary divergence in host-parasite interaction. Of note, significant upregulation of inhibitors of apoptosis (IAPs) was observed in resistant C. gigas but not in susceptible C. virginica, suggesting upregulation of IAPs is an active defense mechanism, not a passive response orchestrated by P. marinus. Compared with C. gigas, C. virginica exhibited greater expansion of toll-like receptors (TLRs) and positive selection in P. marinus responsive TLRs. The C1q domain containing proteins (C1qDCs) with the galactose-binding lectin domain that is involved in P. marinus recognition, were only present and significantly upregulated in C. virginica. These results point to previously undescribed differences in host defense genes between the two oyster species that may account for the difference in susceptibility, providing an expanded portrait of the evolutionary dynamics of host-parasite interaction in lophotrochozoans that lack adaptive immunity. Our findings suggest that C. virginica and P. marinus have a history of coevolution and the recent outbreaks may be due to increased virulence of the parasite.Jiulin ChanJiulin ChanLu WangLu WangLu WangLi LiLi LiLi LiKang MuKang MuKang MuDavid BushekYue XuYue XuXiming GuoGuofan ZhangGuofan ZhangGuofan ZhangLinlin ZhangLinlin ZhangLinlin ZhangFrontiers Media S.A.articleoystercomparative transcriptomicsdermo diseaseinnate immune responsehost-parasiteinteractionGeneticsQH426-470ENFrontiers in Genetics, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	oyster comparative transcriptomics dermo disease innate immune response host-parasite interaction Genetics QH426-470
spellingShingle	oyster comparative transcriptomics dermo disease innate immune response host-parasite interaction Genetics QH426-470 Jiulin Chan Jiulin Chan Lu Wang Lu Wang Lu Wang Li Li Li Li Li Li Kang Mu Kang Mu Kang Mu David Bushek Yue Xu Yue Xu Ximing Guo Guofan Zhang Guofan Zhang Guofan Zhang Linlin Zhang Linlin Zhang Linlin Zhang Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions
description	Infectious disease outbreaks are causing widespread declines of marine invertebrates including corals, sea stars, shrimps, and molluscs. Dermo is a lethal infectious disease of the eastern oyster Crassostrea virginica caused by the protist Perkinsus marinus. The Pacific oyster Crassostrea gigas is resistant to Dermo due to differences in the host-parasite interaction that is not well understood. We compared transcriptomic responses to P. marinus challenge in the two oysters at early and late infection stages. Dynamic and orchestrated regulation of large sets of innate immune response genes were observed in both species with remarkably similar patterns for most orthologs, although responses in C. virginica were stronger, suggesting strong or over-reacting immune response could be a cause of host mortality. Between the two species, several key immune response gene families differed in their expansion, sequence variation and/or transcriptional response to P. marinus, reflecting evolutionary divergence in host-parasite interaction. Of note, significant upregulation of inhibitors of apoptosis (IAPs) was observed in resistant C. gigas but not in susceptible C. virginica, suggesting upregulation of IAPs is an active defense mechanism, not a passive response orchestrated by P. marinus. Compared with C. gigas, C. virginica exhibited greater expansion of toll-like receptors (TLRs) and positive selection in P. marinus responsive TLRs. The C1q domain containing proteins (C1qDCs) with the galactose-binding lectin domain that is involved in P. marinus recognition, were only present and significantly upregulated in C. virginica. These results point to previously undescribed differences in host defense genes between the two oyster species that may account for the difference in susceptibility, providing an expanded portrait of the evolutionary dynamics of host-parasite interaction in lophotrochozoans that lack adaptive immunity. Our findings suggest that C. virginica and P. marinus have a history of coevolution and the recent outbreaks may be due to increased virulence of the parasite.
format	article
author	Jiulin Chan Jiulin Chan Lu Wang Lu Wang Lu Wang Li Li Li Li Li Li Kang Mu Kang Mu Kang Mu David Bushek Yue Xu Yue Xu Ximing Guo Guofan Zhang Guofan Zhang Guofan Zhang Linlin Zhang Linlin Zhang Linlin Zhang
author_facet	Jiulin Chan Jiulin Chan Lu Wang Lu Wang Lu Wang Li Li Li Li Li Li Kang Mu Kang Mu Kang Mu David Bushek Yue Xu Yue Xu Ximing Guo Guofan Zhang Guofan Zhang Guofan Zhang Linlin Zhang Linlin Zhang Linlin Zhang
author_sort	Jiulin Chan
title	Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions
title_short	Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions
title_full	Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions
title_fullStr	Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions
title_full_unstemmed	Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions
title_sort	transcriptomic response to perkinsus marinus in two crassostrea oysters reveals evolutionary dynamics of host-parasite interactions
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/886e83fd6d514cfa82756eaf24e82f9e
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Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions

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