Genomic Analyses of Bifidobacterium moukalabense Reveal Adaptations to Frugivore/Folivore Feeding Behavior

Takahiro Segawa; Satoshi Fukuchi; Dylan Bodington; Sayaka Tsuchida; Pierre Philippe Mbehang Nguema; Hiroshi Mori; Kazunari Ushida

doi:10.3390/microorganisms7040099

Genomic Analyses of Bifidobacterium moukalabense Reveal Adaptations to Frugivore/Folivore Feeding Behavior

Takahiro Segawa, Satoshi Fukuchi, Dylan Bodington, Sayaka Tsuchida, Pierre Philippe Mbehang Nguema, Hiroshi Mori, Kazunari Ushida

Aberdeen Centre For Environmental Sustainability

Research output: Contribution to journal › Article › peer-review

5 Citations (Scopus)

Abstract

Despite the essential role of Bifidobacterium in health-promoting gut bacteria in humans, little is known about their functions in wild animals, especially non-human primates. It is difficult to determine in vivo the function of Bifidobacterium in wild animals due to the limited accessibility of studying target animals in natural conditions. However, the genomic characteristics of Bifidobacterium obtained from the feces of wild animals can provide insight into their functionality in the gut. Here, we analyzed the whole genomes of 12 B. moukalabense strains isolated from seven feces samples of wild western lowland gorillas (Gorilla gorilla gorilla), three samples of wild central chimpanzees (Pan troglodytes troglodytes) and two samples of wild forest elephants (Loxodonta cyclotis) in Moukalaba-Doudou National Park, Gabon. In addition, we analyzed the fecal bacterial communities of six wild western lowland gorillas by meta 16S rRNA gene analyses with next generation sequencing. Although the abundance of the genus Bifidobacterium was as low as 0.2% in the total reads, a whole genome analysis of B. moukalabense suggested its contribution digestion of food and nutrition of frugivore/folivore animals. Specifically, the whole genome analysis indicated the involvement of B. moukalabense in hemicellulose degradation for short chain fatty acid production and nucleic acid utilization as nitrogen resources. In comparison with human-associated Bifidobacterium spp., genes for carbohydrate transport and metabolism are not conserved in these wild species. In particular the glycosidases, which are found in all 12 strains of B. moukalabense, were variably detected, or not detected, in human-associated species.

Original language	English
Number of pages	13
Journal	Microorganisms
Volume	7
Issue number	4
DOIs	https://doi.org/10.3390/microorganisms7040099 https://doi.org/10.3390/microorganisms7040099
Publication status	Published - 4 Apr 2019

Bibliographical note

Funding: This research was funded by the Japan Science and Technology Agency (JST) and Japan International
Cooperation Agency (JICA), grant for the Science and Technology Research Partnership for Sustainable
Development (SATREPS) “Conservation of Biodiversity in Tropical Forest through Sustainable Coexistence
between Human and Wild Animals” (PI, Juichi Yamagiwa) and the study was also supported by Grants-in-Aid
for Scientific Research (15K18775, Sayaka Tsuchida)”.
Acknowledgments: We thank Ayumi Akiyoshi and Chiaki Hagiwara for technical assistance and Takahiro
Yonezawa at Tokyo University of Agriculture for his valuable discussion about genetic evolution of Bifidobacterium.
The authors are indebted for the sampling to Juichi Yamagiwa (Kyoto University), Yuji Takenoshita (Chubu
Gakuin University), Shiho Fujita (Kagoshima University), Ludovic Ngok Banak and Alfred Ngomanda, the former
and the actual Director of the Research Institute of Tropical Ecology (IRET)/National Center of Scientific Research
and Technology (CENAREST) of Gabonese Republic. Takahiro Segawa was supported by Transdisciplinary
Research Integration Center (TRIC) of the Research Organization of Information and Systems. Ortholog analyses
were supported by Basis for Supporting Innovative Drug Discovery and Life Science Research program (2051).
Computations were partially performed on the NIG (National Institute of Genetics) supercomputer at ROIS
(Research Organization of Information and Systems) National Institute of Genetics.

Keywords

Bifidobacterium moukalabense
genomic characteristics
wild chimpanzees
wild forest elephants
wild gorillas

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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title = "Genomic Analyses of Bifidobacterium moukalabense Reveal Adaptations to Frugivore/Folivore Feeding Behavior",

abstract = "Despite the essential role of Bifidobacterium in health-promoting gut bacteria in humans, little is known about their functions in wild animals, especially non-human primates. It is difficult to determine in vivo the function of Bifidobacterium in wild animals due to the limited accessibility of studying target animals in natural conditions. However, the genomic characteristics of Bifidobacterium obtained from the feces of wild animals can provide insight into their functionality in the gut. Here, we analyzed the whole genomes of 12 B. moukalabense strains isolated from seven feces samples of wild western lowland gorillas (Gorilla gorilla gorilla), three samples of wild central chimpanzees (Pan troglodytes troglodytes) and two samples of wild forest elephants (Loxodonta cyclotis) in Moukalaba-Doudou National Park, Gabon. In addition, we analyzed the fecal bacterial communities of six wild western lowland gorillas by meta 16S rRNA gene analyses with next generation sequencing. Although the abundance of the genus Bifidobacterium was as low as 0.2% in the total reads, a whole genome analysis of B. moukalabense suggested its contribution digestion of food and nutrition of frugivore/folivore animals. Specifically, the whole genome analysis indicated the involvement of B. moukalabense in hemicellulose degradation for short chain fatty acid production and nucleic acid utilization as nitrogen resources. In comparison with human-associated Bifidobacterium spp., genes for carbohydrate transport and metabolism are not conserved in these wild species. In particular the glycosidases, which are found in all 12 strains of B. moukalabense, were variably detected, or not detected, in human-associated species.",

keywords = "Bifidobacterium moukalabense, genomic characteristics, wild chimpanzees, wild forest elephants, wild gorillas",

author = "Takahiro Segawa and Satoshi Fukuchi and Dylan Bodington and Sayaka Tsuchida and {Mbehang Nguema}, {Pierre Philippe} and Hiroshi Mori and Kazunari Ushida",

note = "Funding: This research was funded by the Japan Science and Technology Agency (JST) and Japan International Cooperation Agency (JICA), grant for the Science and Technology Research Partnership for Sustainable Development (SATREPS) “Conservation of Biodiversity in Tropical Forest through Sustainable Coexistence between Human and Wild Animals” (PI, Juichi Yamagiwa) and the study was also supported by Grants-in-Aid for Scientific Research (15K18775, Sayaka Tsuchida)”. Acknowledgments: We thank Ayumi Akiyoshi and Chiaki Hagiwara for technical assistance and Takahiro Yonezawa at Tokyo University of Agriculture for his valuable discussion about genetic evolution of Bifidobacterium. The authors are indebted for the sampling to Juichi Yamagiwa (Kyoto University), Yuji Takenoshita (Chubu Gakuin University), Shiho Fujita (Kagoshima University), Ludovic Ngok Banak and Alfred Ngomanda, the former and the actual Director of the Research Institute of Tropical Ecology (IRET)/National Center of Scientific Research and Technology (CENAREST) of Gabonese Republic. Takahiro Segawa was supported by Transdisciplinary Research Integration Center (TRIC) of the Research Organization of Information and Systems. Ortholog analyses were supported by Basis for Supporting Innovative Drug Discovery and Life Science Research program (2051). Computations were partially performed on the NIG (National Institute of Genetics) supercomputer at ROIS (Research Organization of Information and Systems) National Institute of Genetics.",

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doi = "10.3390/microorganisms7040099",

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T1 - Genomic Analyses of Bifidobacterium moukalabense Reveal Adaptations to Frugivore/Folivore Feeding Behavior

AU - Segawa, Takahiro

AU - Fukuchi, Satoshi

AU - Bodington, Dylan

AU - Tsuchida, Sayaka

AU - Mbehang Nguema, Pierre Philippe

AU - Mori, Hiroshi

AU - Ushida, Kazunari

N1 - Funding: This research was funded by the Japan Science and Technology Agency (JST) and Japan International Cooperation Agency (JICA), grant for the Science and Technology Research Partnership for Sustainable Development (SATREPS) “Conservation of Biodiversity in Tropical Forest through Sustainable Coexistence between Human and Wild Animals” (PI, Juichi Yamagiwa) and the study was also supported by Grants-in-Aid for Scientific Research (15K18775, Sayaka Tsuchida)”. Acknowledgments: We thank Ayumi Akiyoshi and Chiaki Hagiwara for technical assistance and Takahiro Yonezawa at Tokyo University of Agriculture for his valuable discussion about genetic evolution of Bifidobacterium. The authors are indebted for the sampling to Juichi Yamagiwa (Kyoto University), Yuji Takenoshita (Chubu Gakuin University), Shiho Fujita (Kagoshima University), Ludovic Ngok Banak and Alfred Ngomanda, the former and the actual Director of the Research Institute of Tropical Ecology (IRET)/National Center of Scientific Research and Technology (CENAREST) of Gabonese Republic. Takahiro Segawa was supported by Transdisciplinary Research Integration Center (TRIC) of the Research Organization of Information and Systems. Ortholog analyses were supported by Basis for Supporting Innovative Drug Discovery and Life Science Research program (2051). Computations were partially performed on the NIG (National Institute of Genetics) supercomputer at ROIS (Research Organization of Information and Systems) National Institute of Genetics.

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N2 - Despite the essential role of Bifidobacterium in health-promoting gut bacteria in humans, little is known about their functions in wild animals, especially non-human primates. It is difficult to determine in vivo the function of Bifidobacterium in wild animals due to the limited accessibility of studying target animals in natural conditions. However, the genomic characteristics of Bifidobacterium obtained from the feces of wild animals can provide insight into their functionality in the gut. Here, we analyzed the whole genomes of 12 B. moukalabense strains isolated from seven feces samples of wild western lowland gorillas (Gorilla gorilla gorilla), three samples of wild central chimpanzees (Pan troglodytes troglodytes) and two samples of wild forest elephants (Loxodonta cyclotis) in Moukalaba-Doudou National Park, Gabon. In addition, we analyzed the fecal bacterial communities of six wild western lowland gorillas by meta 16S rRNA gene analyses with next generation sequencing. Although the abundance of the genus Bifidobacterium was as low as 0.2% in the total reads, a whole genome analysis of B. moukalabense suggested its contribution digestion of food and nutrition of frugivore/folivore animals. Specifically, the whole genome analysis indicated the involvement of B. moukalabense in hemicellulose degradation for short chain fatty acid production and nucleic acid utilization as nitrogen resources. In comparison with human-associated Bifidobacterium spp., genes for carbohydrate transport and metabolism are not conserved in these wild species. In particular the glycosidases, which are found in all 12 strains of B. moukalabense, were variably detected, or not detected, in human-associated species.

AB - Despite the essential role of Bifidobacterium in health-promoting gut bacteria in humans, little is known about their functions in wild animals, especially non-human primates. It is difficult to determine in vivo the function of Bifidobacterium in wild animals due to the limited accessibility of studying target animals in natural conditions. However, the genomic characteristics of Bifidobacterium obtained from the feces of wild animals can provide insight into their functionality in the gut. Here, we analyzed the whole genomes of 12 B. moukalabense strains isolated from seven feces samples of wild western lowland gorillas (Gorilla gorilla gorilla), three samples of wild central chimpanzees (Pan troglodytes troglodytes) and two samples of wild forest elephants (Loxodonta cyclotis) in Moukalaba-Doudou National Park, Gabon. In addition, we analyzed the fecal bacterial communities of six wild western lowland gorillas by meta 16S rRNA gene analyses with next generation sequencing. Although the abundance of the genus Bifidobacterium was as low as 0.2% in the total reads, a whole genome analysis of B. moukalabense suggested its contribution digestion of food and nutrition of frugivore/folivore animals. Specifically, the whole genome analysis indicated the involvement of B. moukalabense in hemicellulose degradation for short chain fatty acid production and nucleic acid utilization as nitrogen resources. In comparison with human-associated Bifidobacterium spp., genes for carbohydrate transport and metabolism are not conserved in these wild species. In particular the glycosidases, which are found in all 12 strains of B. moukalabense, were variably detected, or not detected, in human-associated species.

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DO - 10.3390/microorganisms7040099

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Genomic Analyses of Bifidobacterium moukalabense Reveal Adaptations to Frugivore/Folivore Feeding Behavior

Abstract

Bibliographical note

Keywords

UN SDGs

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