A New ICE clc Subfamily Integrative and Conjugative Element Responsible for Horizontal Transfer of Biphenyl and Salicylic Acid Catabolic Pathway in the PCB-Degrading Strain Pseudomonas stutzeri KF716

Jun Hirose; Takahito Watanabe; Taiki Futagami; Hidehiko Fujihara; Nobutada Kimura; Hikaru Suenaga; Masatoshi Goto; Akiko Suyama; Kensuke Furukawa

doi:10.3390/microorganisms9122462

A New ICE clc Subfamily Integrative and Conjugative Element Responsible for Horizontal Transfer of Biphenyl and Salicylic Acid Catabolic Pathway in the PCB-Degrading Strain Pseudomonas stutzeri KF716

Microorganisms. 2021 Nov 29;9(12):2462. doi: 10.3390/microorganisms9122462.

Authors

Jun Hirose¹, Takahito Watanabe², Taiki Futagami³, Hidehiko Fujihara⁴, Nobutada Kimura⁵, Hikaru Suenaga⁶, Masatoshi Goto⁷, Akiko Suyama⁴, Kensuke Furukawa⁴

Affiliations

¹ Department of Applied Chemistry, Faculty of Engineering, University of Miyazaki, Miyazaki 889-2192, Japan.
² Research Institute for Sustainable Humanosphere, Kyoto University, Uji 611-0011, Japan.
³ Education and Research Center for Fermentation Studies, Faculty of Agriculture, Kagoshima University, Kagoshima 890-0065, Japan.
⁴ Department of Food and Fermentation Sciences, Faculty of Food and Nutrition Sciences, Beppu University, Beppu 874-8501, Japan.
⁵ Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan.
⁶ Cellular and Molecular Biotechnology Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tokyo 135-0064, Japan.
⁷ Faculty of Agriculture, Saga University, Saga 840-8502, Japan.

Abstract

Integrative and conjugative elements (ICEs) are chromosomally integrated self-transmissible mobile genetic elements. Although some ICEs are known to carry genes for the degradation of aromatic compounds, information on their genetic features is limited. We identified a new member of the ICEclc family carrying biphenyl catabolic bph genes and salicylic acid catabolic sal genes from the PCB-degrading strain Pseudomonas stutzeri KF716. The 117-kb ICE_bph-salKF716 contains common core regions exhibiting homology with those of degradative ICEclc from P. knackmussii B13 and ICE_XTD from Azoarcus sp. CIB. A comparison of the gene loci collected from the public database revealed that several putative ICEs from P. putida B6-2, P, alcaliphila JAB1, P. stutzeri AN10, and P. stutzeri 2A20 had highly conserved core regions with those of ICE_bph-salKF716, along with the variable region that encodes the catabolic genes for biphenyl, naphthalene, toluene, or phenol. These data indicate that this type of ICE subfamily is ubiquitously distributed within aromatic compound-degrading bacteria. ICE_bph-salKF716 was transferred from P. stutzeri KF716 to P. aeruginosa PAO1 via a circular extrachromosomal intermediate form. In this study, we describe the structure and genetic features of ICE_bph-salKF716 compared to other catabolic ICEs.

Keywords: ICEXTD; ICEbph-sal; ICEclc; Pseudomonas stutzeri; horizontal gene transfer; integrative and conjugative elements; polychlorinated biphenyls; salicylic acid.