Change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the host

The gut-dwelling microbiota is an indispensable part of termites. It is influenced by a series of factors, such as diet and captivity. The objectives of this study were to study the metabolic functions of hindgut microbiota and to investigate the influence of captivity on the hindgut microbiota. The...

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Main Authors: Most Shormi Alom, Yijing Cen, Rui Tang, Dasong Chen, Hongliang Dou, Zhenzuan Mo, He Du
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Bioengineering and Biotechnology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fbioe.2023.1228918/full
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author Most Shormi Alom
Most Shormi Alom
Yijing Cen
Rui Tang
Dasong Chen
Hongliang Dou
Zhenzuan Mo
Zhenzuan Mo
He Du
author_facet Most Shormi Alom
Most Shormi Alom
Yijing Cen
Rui Tang
Dasong Chen
Hongliang Dou
Zhenzuan Mo
Zhenzuan Mo
He Du
author_sort Most Shormi Alom
collection DOAJ
description The gut-dwelling microbiota is an indispensable part of termites. It is influenced by a series of factors, such as diet and captivity. The objectives of this study were to study the metabolic functions of hindgut microbiota and to investigate the influence of captivity on the hindgut microbiota. The dampwood termite Hodotermopsis sjostedti was reared in the laboratory for 6 months. We conducted the metabolome analysis of the fat body from the freshly-collected workers (FBF), the hindgut fluid of the freshly-collected workers (HFF), and the hindgut fluid of laboratory-maintained workers. In addition, the 16S rRNA genes from the hindgut bacteria in the freshly-collected and laboratory-maintained workers were sequenced. According to our results, the concentrations of metabolites associated with amino acid biosynthesis, vitamin biosynthesis, fatty acid biosynthesis, and cofactor biosynthesis were higher in HFF compared with those in FBF, suggesting that the hindgut microbiota provides nutritional factors to the host. However, after captivity, the concentrations of metabolites in the hindgut associated with amino acid biosynthesis, nucleotide sugar metabolism, vitamin biosynthesis, and carbon metabolism decreased, while those associated with the steroid hormone biosynthesis and ovarian steroidogenesis increased. Meanwhile, the 16S amplicon study revealed that the abundance of certain bacteria changed after captivity, such as uncultured Termite Group 1 bacterium, Candidatus Symbiothrix dinenymphae, and unclassified Desulfovibrio. Our findings show that captivity influences the hindgut microbiota and shed light on the metabolic potential of the hindgut microbiota.
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spelling doaj.art-a45a376df42742e69fbfd2131607ec132024-01-15T11:02:27ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852024-01-011110.3389/fbioe.2023.12289181228918Change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the hostMost Shormi Alom0Most Shormi Alom1Yijing Cen2Rui Tang3Dasong Chen4Hongliang Dou5Zhenzuan Mo6Zhenzuan Mo7He Du8Guangdong Key Laboratory of Integrated Pest Management in Agriculture, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaGuangdong Key Laboratory of Integrated Pest Management in Agriculture, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, ChinaGuangdong Key Laboratory of Integrated Pest Management in Agriculture, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou, ChinaGuangdong Key Laboratory of Integrated Pest Management in Agriculture, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaGuangdong Key Laboratory of Integrated Pest Management in Agriculture, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, ChinaThe gut-dwelling microbiota is an indispensable part of termites. It is influenced by a series of factors, such as diet and captivity. The objectives of this study were to study the metabolic functions of hindgut microbiota and to investigate the influence of captivity on the hindgut microbiota. The dampwood termite Hodotermopsis sjostedti was reared in the laboratory for 6 months. We conducted the metabolome analysis of the fat body from the freshly-collected workers (FBF), the hindgut fluid of the freshly-collected workers (HFF), and the hindgut fluid of laboratory-maintained workers. In addition, the 16S rRNA genes from the hindgut bacteria in the freshly-collected and laboratory-maintained workers were sequenced. According to our results, the concentrations of metabolites associated with amino acid biosynthesis, vitamin biosynthesis, fatty acid biosynthesis, and cofactor biosynthesis were higher in HFF compared with those in FBF, suggesting that the hindgut microbiota provides nutritional factors to the host. However, after captivity, the concentrations of metabolites in the hindgut associated with amino acid biosynthesis, nucleotide sugar metabolism, vitamin biosynthesis, and carbon metabolism decreased, while those associated with the steroid hormone biosynthesis and ovarian steroidogenesis increased. Meanwhile, the 16S amplicon study revealed that the abundance of certain bacteria changed after captivity, such as uncultured Termite Group 1 bacterium, Candidatus Symbiothrix dinenymphae, and unclassified Desulfovibrio. Our findings show that captivity influences the hindgut microbiota and shed light on the metabolic potential of the hindgut microbiota.https://www.frontiersin.org/articles/10.3389/fbioe.2023.1228918/fullsymbiosisnitrogen economymetaboliterearing conditionuricolytic bacteria
spellingShingle Most Shormi Alom
Most Shormi Alom
Yijing Cen
Rui Tang
Dasong Chen
Hongliang Dou
Zhenzuan Mo
Zhenzuan Mo
He Du
Change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the host
Frontiers in Bioengineering and Biotechnology
symbiosis
nitrogen economy
metabolite
rearing condition
uricolytic bacteria
title Change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the host
title_full Change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the host
title_fullStr Change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the host
title_full_unstemmed Change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the host
title_short Change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the host
title_sort change of termite hindgut metabolome and bacteria after captivity indicates the hindgut microbiota provides nutritional factors to the host
topic symbiosis
nitrogen economy
metabolite
rearing condition
uricolytic bacteria
url https://www.frontiersin.org/articles/10.3389/fbioe.2023.1228918/full
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