Prokaryotic and viral genomes recovered from 787 Japanese gut metagenomes revealed microbial features linked to diets, populations, and diseases

Yoshihiko Tomofuji; Toshihiro Kishikawa; Yuichi Maeda; Kotaro Ogawa; Yuriko Otake-Kasamoto; Shuhei Kawabata; Takuro Nii; Tatsusada Okuno; Eri Oguro-Igashira; Makoto Kinoshita; Masatoshi Takagaki; Naoki Oyama; Kenichi Todo; Kenichi Yamamoto; Kyuto Sonehara; Mayu Yagita; Akiko Hosokawa; Daisuke Motooka; Yuki Matsumoto; Hidetoshi Matsuoka; Maiko Yoshimura; Shiro Ohshima; Shinichiro Shinzaki; Shota Nakamura; Hideki Iijima; Hidenori Inohara; Haruhiko Kishima; Tetsuo Takehara; Hideki Mochizuki; Kiyoshi Takeda; Atsushi Kumanogoh; Yukinori Okada

doi:10.1016/j.xgen.2022.100219

Prokaryotic and viral genomes recovered from 787 Japanese gut metagenomes revealed microbial features linked to diets, populations, and diseases

Cell Genom. 2022 Nov 30;2(12):100219. doi: 10.1016/j.xgen.2022.100219. eCollection 2022 Dec 14.

Authors

Yoshihiko Tomofuji^{1

2}, Toshihiro Kishikawa^{1

3

4}, Yuichi Maeda^{2

5

6}, Kotaro Ogawa⁷, Yuriko Otake-Kasamoto⁸, Shuhei Kawabata⁹, Takuro Nii^{5

6}, Tatsusada Okuno⁷, Eri Oguro-Igashira^{5

6}, Makoto Kinoshita⁷, Masatoshi Takagaki⁹, Naoki Oyama¹⁰, Kenichi Todo⁷, Kenichi Yamamoto^{1

11

12}, Kyuto Sonehara^{1

2}, Mayu Yagita^{5

6}, Akiko Hosokawa¹³, Daisuke Motooka^{2

14}, Yuki Matsumoto¹⁴, Hidetoshi Matsuoka¹⁵, Maiko Yoshimura¹⁵, Shiro Ohshima¹⁵, Shinichiro Shinzaki⁸, Shota Nakamura^{2

14}, Hideki Iijima⁸, Hidenori Inohara³, Haruhiko Kishima⁹, Tetsuo Takehara⁸, Hideki Mochizuki⁷, Kiyoshi Takeda^{6

16}, Atsushi Kumanogoh^{2

5

17}, Yukinori Okada^{1

2

12

18

19

20}

Affiliations

¹ Department of Statistical Genetics, Osaka University Graduate School of Medicine, 2-2 Yamadaoka, Suita 565-0871, Japan.
² Integrated Frontier Research for Medical Science Division, Institute for Open and Transdisciplinary Research Initiatives, Osaka University, Suita 565-0871, Japan.
³ Department of Otorhinolaryngology-Head and Neck Surgery, Osaka University Graduate School of Medicine, Suita 565-0871, Japan.
⁴ Department of Head and Neck Surgery, Aichi Cancer Center Hospital, Nagoya 464-8681, Japan.
⁵ Department of Respiratory Medicine and Clinical Immunology, Osaka University Graduate School of Medicine, Suita 565-0871, Japan.
⁶ Laboratory of Immune Regulation, Department of Microbiology and Immunology, Osaka University Graduate School of Medicine, Suita 565-0871, Japan.
⁷ Department of Neurology, Osaka University Graduate School of Medicine, Suita 565-0871, Japan.
⁸ Department of Gastroenterology and Hepatology, Osaka University Graduate School of Medicine, Suita 565-0871, Japan.
⁹ Department of Neurosurgery, Osaka University Graduate School of Medicine, Suita 565-0871, Japan.
¹⁰ Department of Stroke Medicine, Kawasaki Medical School, Kurashiki 701-0192, Japan.
¹¹ Department of Pediatrics, Osaka University Graduate School of Medicine, Suita 565-0871, Japan.
¹² Laboratory of Statistical Immunology, Immunology Frontier Research Center (WPI-IFReC), Osaka University, Suita 565-0871, Japan.
¹³ Department of Neurology, Suita Municipal Hospital, Suita 564-8567, Japan.
¹⁴ Department of Infection Metagenomics, Research Institute for Microbial Diseases, Osaka University, Suita 565-0871, Japan.
¹⁵ Department of Rheumatology and Allergology, NHO Osaka Minami Medical Center, Kawachinagano 586-8521, Japan.
¹⁶ WPI Immunology Frontier Research Center, Osaka University, Suita 565-0871, Japan.
¹⁷ Department of Immunopathology, Immunology Frontier Research Center, Osaka University, Suita 565-0871, Japan.
¹⁸ Laboratory for Systems Genetics, RIKEN Center for Integrative Medical Sciences, Tsurumi 230-0045, Japan.
¹⁹ Center for Infectious Disease Education and Research, Osaka University, Suita 565-0871, Japan.
²⁰ Department of Genome Informatics, Graduate School of Medicine, the University of Tokyo, Tokyo, Japan.

Abstract

We reconstructed 19,084 prokaryotic and 31,395 viral genomes from 787 Japanese gut metagenomes as Japanese metagenome-assembled genomes (JMAG) and Japanese Virus Database (JVD), which are large microbial genome datasets for a single population. Population-specific enrichment of the Bacillus subtilis and β-porphyranase among the JMAG could derive from the Japanese traditional food natto (fermented soybeans) and nori (laver), respectively. Dairy-related Enterococcus_B lactis and Streptococcus thermophilus were nominally associated with the East Asian-specific missense variant rs671:G>A in ALDH2, which was associated with dairy consumption. Of the species-level viral genome clusters in the JVD, 62.9% were novel. The β crAss-like phage composition was low among the Japanese but relatively high among African and Oceanian peoples. Evaluations of the association between crAss-like phages and diseases showed significant disease-specific associations. Our large catalog of virus-host pairs identified the positive correlation between the abundance of the viruses and their hosts.

Keywords: database; gut microbe; metagenome-assembled genome; prokaryotic genome; viral genome.