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Whole-genome analysis of the colonization-resistant bacterium Phytobacter sp. SCO41T isolated from Bacillus nematocida B16-fed adult Caenorhabditis elegans

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Abstract

Colonization resistance is an important attribute for bacterial interactions with hosts, but the mechanism is still not completely clear. In this study, we found that Phytobacter sp. SCO41T can effectively inhibit the in vivo colonization of Bacillus nematocida B16 in Caenorhabditis elegans, and we revealed the colonization resistance mechanism. Three strains of colonization-resistant bacteria, SCO41T, BX15, and BC7, were isolated from the intestines of the free-living nematode C. elegans derived from rotten fruit and soil. The primary characteristics and genome map of one of the three isolates was investigated to explore the underlying mechanism of colonization resistance in C. elegans. In addition, we performed exogenous iron supplementation and gene cluster knockout experiments to validate the sequencing results. The results showed that relationship was close among the three strains, which was identified as belonging to the genus Phytobacter. The type strain is SCO41T (= CICC 24103T = KCTC 52362T). Whole genome analysis showed that csgA, csgB, csgC, csgE, csgF, and csgG were involved in the curli adhesive process and that fepA, fepB, fepC, fepD, and fepG played important roles in SCO41T against the colonization of B. nematocida B16 in C. elegans by competing for iron. Exogenous iron supplementation showed that exogenous iron can increase the colonization of B. nematocida B16, which was additionally confirmed by a deletion mutant strain. The csg gene family contributes to the colonization of SCO41T in C. elegans. Curli potentially contribute to the colonization of SCO41T in C. elegans, and enterobactin has a key role in SCO41T to resist the colonization of B. nematocida B16 by competing for iron.

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Acknowledgements

This work was supported by the projects from the National Natural Science Foundation Program of the People’s Republic of China (Grant Nos. 31770138, 31570120 31100104 and 31870917) and by program for Science & Technology Innovation Talents in Universities of Henan province, HASTIT (Grant No. 17HASTIT041) and by the fund of Scientific and Technological research project of Henan province (Grant No. 182102110084).

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  1. Bowen Wang and Bingfen Huang contributed equally to the work.

Authors and Affiliations

  1. Department of Life Science and Biotechnology, Nanyang Normal University, Nanyang, 473000, People’s Republic of China

    Bowen Wang, Bingfen Huang, Junmei Chen, Wenpeng Li & Qiuhong Niu

  2. Nanyang Academy of Agricultural Sciences, Nanyang, 473083, Henan, People’s Republic of China

    Ling Yang

  3. Henan Key Laboratory of Ecological Security for Water Source Region of Mid-line of South-to-North Diversion Project of Henan Province, Nanyang, People’s Republic of China

    Lunguang Yao

  4. China-UK-NYNU-RRes Joint Laboratory of Insect Biology, Nanyang Normal University, Nanyang, 473000, People’s Republic of China

    Qiuhong Niu

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  1. Bowen Wang
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Contributions

QHN and LGY conceived and designed the experiments. BWW and BFH performed the bacterial isolation and the final genome assembly, analyzed the genome annotation. JMC and WPL carried out the characterizations and classification of the bacterial strains. LY coordinated the sequence analysis and the drafted the manuscript. LGY, QHN, BWW, and BFH participated in the verification experiments, and helped draft the manuscript. All authors read and approved the final manuscript.

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Correspondence to Lunguang Yao or Qiuhong Niu.

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Wang, B., Huang, B., Chen, J. et al. Whole-genome analysis of the colonization-resistant bacterium Phytobacter sp. SCO41T isolated from Bacillus nematocida B16-fed adult Caenorhabditis elegans. Mol Biol Rep 46, 1563–1575 (2019). https://doi.org/10.1007/s11033-018-04574-w

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