Complete genome sequence of bradyrhizobium sp. S23321: Insights into symbiosis evolution in soil oligotrophs

Takashi Okubo, Takahiro Tsukui, Hiroko Maita, Shinobu Okamoto, Kenshiro Oshima, Takatomo Fujisawa, Akihiro Saito, Hiroyuki Futamata, Reiko Hattori, Yumi Shimomura, Shin Haruta, Sho Morimoto, Yong Wang, Yoriko Sakai, Masahira Hattori, Shin Ichi Aizawa, Kenji V P Nagashima, Sachiko Masuda, Tsutomu Hattori, Akifumi YamashitaZhihua Bao, Masahito Hayatsu, Hiromi Kajiya-Kanegae, Ikuo Yoshinaga, Kazunori Sakamoto, Koki Toyota, Mitsuteru Nakao, Mitsuyo Kohara, Mizue Anda, Rieko Niwa, Park Jung-Hwan, Reiko Sameshima-Saito, Shin Ichi Tokuda, Sumiko Yamamoto, Syuji Yamamoto, Tadashi Yokoyama, Tomoko Akutsu, Yasukazu Nakamura, Yuka Nakahira-Yanaka, Yuko Takada Hoshino, Hideki Hirakawa, Hisayuki Mitsui, Kimihiro Terasawa, Manabu Itakura, Shusei Sato, Wakako Ikeda-Ohtsubo, Natsuko Sakakura, Eli Kaminuma, Kiwamu Minamisawa

Research output: Contribution to journalArticle

33 Citations (Scopus)

Abstract

Bradyrhizobium sp. S23321 is an oligotrophic bacterium isolated from paddy field soil. Although S23321 is phylogenetically close to Bradyrhizobium japonicum USDA110, a legume symbiont, it is unable to induce root nodules in siratro, a legume often used for testing Nod factor-dependent nodulation. The genome of S23321 is a single circular chromosome, 7,231,841 bp in length, with an average GC content of 64.3%. The genome contains 6,898 potential protein-encoding genes, one set of rRNA genes, and 45 tRNA genes. Comparison of the genome structure between S23321 and USDA110 showed strong colinearity; however, the symbiosis islands present in USDA110 were absent in S23321, whose genome lacked a chaperonin gene cluster (groELS3) for symbiosis regulation found in USDA110. A comparison of sequences around the tRNA-Val gene strongly suggested that S23321 contains an ancestral-type genome that precedes the acquisition of a symbiosis island by horizontal gene transfer. Although S23321 contains a nif (nitrogen fixation) gene cluster, the organization, homology, and phylogeny of the genes in this cluster were more similar to those of photosynthetic bradyrhizobia ORS278 and BTAi1 than to those on the symbiosis island of USDA110. In addition, we found genes encoding a complete photosynthetic system, many ABC transporters for amino acids and oligopeptides, two types (polar and lateral) of flagella, multiple respiratory chains, and a system for lignin monomer catabolism in the S23321 genome. These features suggest that S23321 is able to adapt to a wide range of environments, probably including low-nutrient conditions, with multiple survival strategies in soil and rhizosphere.

Original languageEnglish
Pages (from-to)306-315
Number of pages10
JournalMicrobes and Environments
Volume27
Issue number3
DOIs
Publication statusPublished - 2012
Externally publishedYes

Fingerprint

Bradyrhizobium
soil formation
symbiosis
genome
genomic islands
gene
multigene family
soil
genes
Photorhizobium
legumes
Macroptilium atropurpureum
chaperonins
oligopeptides
ABC transporters
Bradyrhizobium japonicum
electron transport chain
root nodules
flagellum
nodulation

Keywords

  • Bradyrhizobium sp. S23321
  • Comparative genomics
  • Oligotrophic soil bacterium
  • Photosynthesis
  • Symbiosis evolution

ASJC Scopus subject areas

  • Plant Science
  • Soil Science
  • Ecology, Evolution, Behavior and Systematics

Cite this

Okubo, T., Tsukui, T., Maita, H., Okamoto, S., Oshima, K., Fujisawa, T., ... Minamisawa, K. (2012). Complete genome sequence of bradyrhizobium sp. S23321: Insights into symbiosis evolution in soil oligotrophs. Microbes and Environments, 27(3), 306-315. https://doi.org/10.1264/jsme2.ME11321

Complete genome sequence of bradyrhizobium sp. S23321 : Insights into symbiosis evolution in soil oligotrophs. / Okubo, Takashi; Tsukui, Takahiro; Maita, Hiroko; Okamoto, Shinobu; Oshima, Kenshiro; Fujisawa, Takatomo; Saito, Akihiro; Futamata, Hiroyuki; Hattori, Reiko; Shimomura, Yumi; Haruta, Shin; Morimoto, Sho; Wang, Yong; Sakai, Yoriko; Hattori, Masahira; Aizawa, Shin Ichi; Nagashima, Kenji V P; Masuda, Sachiko; Hattori, Tsutomu; Yamashita, Akifumi; Bao, Zhihua; Hayatsu, Masahito; Kajiya-Kanegae, Hiromi; Yoshinaga, Ikuo; Sakamoto, Kazunori; Toyota, Koki; Nakao, Mitsuteru; Kohara, Mitsuyo; Anda, Mizue; Niwa, Rieko; Jung-Hwan, Park; Sameshima-Saito, Reiko; Tokuda, Shin Ichi; Yamamoto, Sumiko; Yamamoto, Syuji; Yokoyama, Tadashi; Akutsu, Tomoko; Nakamura, Yasukazu; Nakahira-Yanaka, Yuka; Hoshino, Yuko Takada; Hirakawa, Hideki; Mitsui, Hisayuki; Terasawa, Kimihiro; Itakura, Manabu; Sato, Shusei; Ikeda-Ohtsubo, Wakako; Sakakura, Natsuko; Kaminuma, Eli; Minamisawa, Kiwamu.

In: Microbes and Environments, Vol. 27, No. 3, 2012, p. 306-315.

Research output: Contribution to journalArticle

Okubo, T, Tsukui, T, Maita, H, Okamoto, S, Oshima, K, Fujisawa, T, Saito, A, Futamata, H, Hattori, R, Shimomura, Y, Haruta, S, Morimoto, S, Wang, Y, Sakai, Y, Hattori, M, Aizawa, SI, Nagashima, KVP, Masuda, S, Hattori, T, Yamashita, A, Bao, Z, Hayatsu, M, Kajiya-Kanegae, H, Yoshinaga, I, Sakamoto, K, Toyota, K, Nakao, M, Kohara, M, Anda, M, Niwa, R, Jung-Hwan, P, Sameshima-Saito, R, Tokuda, SI, Yamamoto, S, Yamamoto, S, Yokoyama, T, Akutsu, T, Nakamura, Y, Nakahira-Yanaka, Y, Hoshino, YT, Hirakawa, H, Mitsui, H, Terasawa, K, Itakura, M, Sato, S, Ikeda-Ohtsubo, W, Sakakura, N, Kaminuma, E & Minamisawa, K 2012, 'Complete genome sequence of bradyrhizobium sp. S23321: Insights into symbiosis evolution in soil oligotrophs', Microbes and Environments, vol. 27, no. 3, pp. 306-315. https://doi.org/10.1264/jsme2.ME11321
Okubo, Takashi ; Tsukui, Takahiro ; Maita, Hiroko ; Okamoto, Shinobu ; Oshima, Kenshiro ; Fujisawa, Takatomo ; Saito, Akihiro ; Futamata, Hiroyuki ; Hattori, Reiko ; Shimomura, Yumi ; Haruta, Shin ; Morimoto, Sho ; Wang, Yong ; Sakai, Yoriko ; Hattori, Masahira ; Aizawa, Shin Ichi ; Nagashima, Kenji V P ; Masuda, Sachiko ; Hattori, Tsutomu ; Yamashita, Akifumi ; Bao, Zhihua ; Hayatsu, Masahito ; Kajiya-Kanegae, Hiromi ; Yoshinaga, Ikuo ; Sakamoto, Kazunori ; Toyota, Koki ; Nakao, Mitsuteru ; Kohara, Mitsuyo ; Anda, Mizue ; Niwa, Rieko ; Jung-Hwan, Park ; Sameshima-Saito, Reiko ; Tokuda, Shin Ichi ; Yamamoto, Sumiko ; Yamamoto, Syuji ; Yokoyama, Tadashi ; Akutsu, Tomoko ; Nakamura, Yasukazu ; Nakahira-Yanaka, Yuka ; Hoshino, Yuko Takada ; Hirakawa, Hideki ; Mitsui, Hisayuki ; Terasawa, Kimihiro ; Itakura, Manabu ; Sato, Shusei ; Ikeda-Ohtsubo, Wakako ; Sakakura, Natsuko ; Kaminuma, Eli ; Minamisawa, Kiwamu. / Complete genome sequence of bradyrhizobium sp. S23321 : Insights into symbiosis evolution in soil oligotrophs. In: Microbes and Environments. 2012 ; Vol. 27, No. 3. pp. 306-315.
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abstract = "Bradyrhizobium sp. S23321 is an oligotrophic bacterium isolated from paddy field soil. Although S23321 is phylogenetically close to Bradyrhizobium japonicum USDA110, a legume symbiont, it is unable to induce root nodules in siratro, a legume often used for testing Nod factor-dependent nodulation. The genome of S23321 is a single circular chromosome, 7,231,841 bp in length, with an average GC content of 64.3{\%}. The genome contains 6,898 potential protein-encoding genes, one set of rRNA genes, and 45 tRNA genes. Comparison of the genome structure between S23321 and USDA110 showed strong colinearity; however, the symbiosis islands present in USDA110 were absent in S23321, whose genome lacked a chaperonin gene cluster (groELS3) for symbiosis regulation found in USDA110. A comparison of sequences around the tRNA-Val gene strongly suggested that S23321 contains an ancestral-type genome that precedes the acquisition of a symbiosis island by horizontal gene transfer. Although S23321 contains a nif (nitrogen fixation) gene cluster, the organization, homology, and phylogeny of the genes in this cluster were more similar to those of photosynthetic bradyrhizobia ORS278 and BTAi1 than to those on the symbiosis island of USDA110. In addition, we found genes encoding a complete photosynthetic system, many ABC transporters for amino acids and oligopeptides, two types (polar and lateral) of flagella, multiple respiratory chains, and a system for lignin monomer catabolism in the S23321 genome. These features suggest that S23321 is able to adapt to a wide range of environments, probably including low-nutrient conditions, with multiple survival strategies in soil and rhizosphere.",
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T1 - Complete genome sequence of bradyrhizobium sp. S23321

T2 - Insights into symbiosis evolution in soil oligotrophs

AU - Okubo, Takashi

AU - Tsukui, Takahiro

AU - Maita, Hiroko

AU - Okamoto, Shinobu

AU - Oshima, Kenshiro

AU - Fujisawa, Takatomo

AU - Saito, Akihiro

AU - Futamata, Hiroyuki

AU - Hattori, Reiko

AU - Shimomura, Yumi

AU - Haruta, Shin

AU - Morimoto, Sho

AU - Wang, Yong

AU - Sakai, Yoriko

AU - Hattori, Masahira

AU - Aizawa, Shin Ichi

AU - Nagashima, Kenji V P

AU - Masuda, Sachiko

AU - Hattori, Tsutomu

AU - Yamashita, Akifumi

AU - Bao, Zhihua

AU - Hayatsu, Masahito

AU - Kajiya-Kanegae, Hiromi

AU - Yoshinaga, Ikuo

AU - Sakamoto, Kazunori

AU - Toyota, Koki

AU - Nakao, Mitsuteru

AU - Kohara, Mitsuyo

AU - Anda, Mizue

AU - Niwa, Rieko

AU - Jung-Hwan, Park

AU - Sameshima-Saito, Reiko

AU - Tokuda, Shin Ichi

AU - Yamamoto, Sumiko

AU - Yamamoto, Syuji

AU - Yokoyama, Tadashi

AU - Akutsu, Tomoko

AU - Nakamura, Yasukazu

AU - Nakahira-Yanaka, Yuka

AU - Hoshino, Yuko Takada

AU - Hirakawa, Hideki

AU - Mitsui, Hisayuki

AU - Terasawa, Kimihiro

AU - Itakura, Manabu

AU - Sato, Shusei

AU - Ikeda-Ohtsubo, Wakako

AU - Sakakura, Natsuko

AU - Kaminuma, Eli

AU - Minamisawa, Kiwamu

PY - 2012

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AB - Bradyrhizobium sp. S23321 is an oligotrophic bacterium isolated from paddy field soil. Although S23321 is phylogenetically close to Bradyrhizobium japonicum USDA110, a legume symbiont, it is unable to induce root nodules in siratro, a legume often used for testing Nod factor-dependent nodulation. The genome of S23321 is a single circular chromosome, 7,231,841 bp in length, with an average GC content of 64.3%. The genome contains 6,898 potential protein-encoding genes, one set of rRNA genes, and 45 tRNA genes. Comparison of the genome structure between S23321 and USDA110 showed strong colinearity; however, the symbiosis islands present in USDA110 were absent in S23321, whose genome lacked a chaperonin gene cluster (groELS3) for symbiosis regulation found in USDA110. A comparison of sequences around the tRNA-Val gene strongly suggested that S23321 contains an ancestral-type genome that precedes the acquisition of a symbiosis island by horizontal gene transfer. Although S23321 contains a nif (nitrogen fixation) gene cluster, the organization, homology, and phylogeny of the genes in this cluster were more similar to those of photosynthetic bradyrhizobia ORS278 and BTAi1 than to those on the symbiosis island of USDA110. In addition, we found genes encoding a complete photosynthetic system, many ABC transporters for amino acids and oligopeptides, two types (polar and lateral) of flagella, multiple respiratory chains, and a system for lignin monomer catabolism in the S23321 genome. These features suggest that S23321 is able to adapt to a wide range of environments, probably including low-nutrient conditions, with multiple survival strategies in soil and rhizosphere.

KW - Bradyrhizobium sp. S23321

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KW - Oligotrophic soil bacterium

KW - Photosynthesis

KW - Symbiosis evolution

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