A Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle

ABSTRACT The saw-toothed grain beetle, Oryzaephilus surinamensis (Silvanidae), is a cosmopolitan stored-product pest. Early studies on O. surinamensis in the 1930s described the presence of peculiar bacteriomes harboring endosymbiotic bacteria in the abdomen. Since then, however, the microbiological...

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Autores principales:	Bin Hirota, Genta Okude, Hisashi Anbutsu, Ryo Futahashi, Minoru Moriyama, Xian-Ying Meng, Naruo Nikoh, Ryuichi Koga, Takema Fukatsu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	bacterial symbiont bacteriocyte bacteriome Bacteroidetes cuticle formation Oryzaephilus surinamensis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3ac7125d92614e6f823b7938099f4256
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spelling	oai:doaj.org-article:3ac7125d92614e6f823b7938099f42562021-11-15T15:51:50ZA Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle10.1128/mBio.01482-172150-7511https://doaj.org/article/3ac7125d92614e6f823b7938099f42562017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01482-17https://doaj.org/toc/2150-7511ABSTRACT The saw-toothed grain beetle, Oryzaephilus surinamensis (Silvanidae), is a cosmopolitan stored-product pest. Early studies on O. surinamensis in the 1930s described the presence of peculiar bacteriomes harboring endosymbiotic bacteria in the abdomen. Since then, however, the microbiological nature of the symbiont has been elusive. Here we investigated the endosymbiotic system of O. surinamensis in detail. In the abdomen of adults, pupae, and larvae, four oval bacteriomes were consistently identified, whose cytoplasm was full of extremely elongated tubular bacterial cells several micrometers wide and several hundred micrometers long. Molecular phylogenetic analysis identified the symbiont as a member of the Bacteroidetes, in which the symbiont was the most closely related to the endosymbiont of a grain pest beetle, Rhyzopertha dominica (Bostrichidae). The symbiont was detected in developing embryos, corroborating vertical symbiont transmission through host generations. The symbiont gene showed AT-biased nucleotide composition and accelerated molecular evolution, plausibly reflecting degenerative evolution of the symbiont genome. When the symbiont infection was experimentally removed, the aposymbiotic insects grew and reproduced normally, but exhibited a slightly but significantly more reddish cuticle and lighter body mass. These results indicate that the symbiont of O. surinamensis is not essential for the host’s growth and reproduction but contributes to the host’s cuticle formation. Symbiont genome sequencing and detailed comparison of fitness parameters between symbiotic and aposymbiotic insects under various environmental conditions will provide further insights into the symbiont’s biological roles for the stored-product pest. IMPORTANCE Some beetles notorious as stored-product pests possess well-developed symbiotic organs called bacteriomes for harboring specific symbiotic bacteria, although their biological roles have been poorly understood. Here we report a peculiar endosymbiotic system of a grain pest beetle, Oryzaephilus surinamensis, in which four oval bacteriomes in the abdomen are full of extremely elongated tubular bacterial cells. Experimental symbiont elimination did not hinder the host’s growth and reproduction, but resulted in emergence of reddish beetles, uncovering the symbiont’s involvement in host’s cuticle formation. We speculate that the extremely elongated symbiont cell morphology might be due to the degenerative symbiont genome deficient in bacterial cell division and/or cell wall formation, which highlights an evolutionary consequence of intimate host-symbiont coevolution.Bin HirotaGenta OkudeHisashi AnbutsuRyo FutahashiMinoru MoriyamaXian-Ying MengNaruo NikohRyuichi KogaTakema FukatsuAmerican Society for Microbiologyarticlebacterial symbiontbacteriocytebacteriomeBacteroidetescuticle formationOryzaephilus surinamensisMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacterial symbiont bacteriocyte bacteriome Bacteroidetes cuticle formation Oryzaephilus surinamensis Microbiology QR1-502
spellingShingle	bacterial symbiont bacteriocyte bacteriome Bacteroidetes cuticle formation Oryzaephilus surinamensis Microbiology QR1-502 Bin Hirota Genta Okude Hisashi Anbutsu Ryo Futahashi Minoru Moriyama Xian-Ying Meng Naruo Nikoh Ryuichi Koga Takema Fukatsu A Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle
description	ABSTRACT The saw-toothed grain beetle, Oryzaephilus surinamensis (Silvanidae), is a cosmopolitan stored-product pest. Early studies on O. surinamensis in the 1930s described the presence of peculiar bacteriomes harboring endosymbiotic bacteria in the abdomen. Since then, however, the microbiological nature of the symbiont has been elusive. Here we investigated the endosymbiotic system of O. surinamensis in detail. In the abdomen of adults, pupae, and larvae, four oval bacteriomes were consistently identified, whose cytoplasm was full of extremely elongated tubular bacterial cells several micrometers wide and several hundred micrometers long. Molecular phylogenetic analysis identified the symbiont as a member of the Bacteroidetes, in which the symbiont was the most closely related to the endosymbiont of a grain pest beetle, Rhyzopertha dominica (Bostrichidae). The symbiont was detected in developing embryos, corroborating vertical symbiont transmission through host generations. The symbiont gene showed AT-biased nucleotide composition and accelerated molecular evolution, plausibly reflecting degenerative evolution of the symbiont genome. When the symbiont infection was experimentally removed, the aposymbiotic insects grew and reproduced normally, but exhibited a slightly but significantly more reddish cuticle and lighter body mass. These results indicate that the symbiont of O. surinamensis is not essential for the host’s growth and reproduction but contributes to the host’s cuticle formation. Symbiont genome sequencing and detailed comparison of fitness parameters between symbiotic and aposymbiotic insects under various environmental conditions will provide further insights into the symbiont’s biological roles for the stored-product pest. IMPORTANCE Some beetles notorious as stored-product pests possess well-developed symbiotic organs called bacteriomes for harboring specific symbiotic bacteria, although their biological roles have been poorly understood. Here we report a peculiar endosymbiotic system of a grain pest beetle, Oryzaephilus surinamensis, in which four oval bacteriomes in the abdomen are full of extremely elongated tubular bacterial cells. Experimental symbiont elimination did not hinder the host’s growth and reproduction, but resulted in emergence of reddish beetles, uncovering the symbiont’s involvement in host’s cuticle formation. We speculate that the extremely elongated symbiont cell morphology might be due to the degenerative symbiont genome deficient in bacterial cell division and/or cell wall formation, which highlights an evolutionary consequence of intimate host-symbiont coevolution.
format	article
author	Bin Hirota Genta Okude Hisashi Anbutsu Ryo Futahashi Minoru Moriyama Xian-Ying Meng Naruo Nikoh Ryuichi Koga Takema Fukatsu
author_facet	Bin Hirota Genta Okude Hisashi Anbutsu Ryo Futahashi Minoru Moriyama Xian-Ying Meng Naruo Nikoh Ryuichi Koga Takema Fukatsu
author_sort	Bin Hirota
title	A Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle
title_short	A Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle
title_full	A Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle
title_fullStr	A Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle
title_full_unstemmed	A Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle
title_sort	novel, extremely elongated, and endocellular bacterial symbiont supports cuticle formation of a grain pest beetle
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/3ac7125d92614e6f823b7938099f4256
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A Novel, Extremely Elongated, and Endocellular Bacterial Symbiont Supports Cuticle Formation of a Grain Pest Beetle

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