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Applied Microbiology and Biotechnology

, Volume 103, Issue 11, pp 4499–4510 | Cite as

Co-occurrence of functional modules derived from nicotine-degrading gene clusters confers additive effects in Pseudomonas sp. JY-Q

  • Jun Li
  • Jie Wang
  • Shanshan Li
  • Fengmei Yi
  • Jian Xu
  • Ming ShuEmail author
  • Mingjie Shen
  • Yang Jiao
  • Feng Tao
  • Chengyun Zhu
  • Hui Zhang
  • Shulan Qian
  • Weihong ZhongEmail author
Genomics, transcriptomics, proteomics

Abstract

Pseudomonas sp. JY-Q was isolated from nicotine-rich environment and could degrade and tolerate high-content nicotine. Its specific genetic architecture comprised duplicated homologous nicotine-degrading clusters for different functional modules on the whole pathway. Its adaptive and genomic properties caused our concern whether the duplicated homologous gene clusters confer additive effects on nicotine degradation and result in strain JY-Q strong capability. After deletion of representative genes from duplicated homologous gene clusters of upstream module Nic1, midstream module Spm, and downstream module Nic2, the nicotine degradation efficiency of the wild type and mutant strains were examined. As the first genes of clusters Nic1-1 and Nic1-2, nicA2 and nox are both involved in nicotine degradation, but nox exhibited more contribution to nicotine metabolism due to the higher transcriptional amount of nox than that of nicA2. Likewise, the sub-clusters spm1 and spm2 showed additive effect on nicotine metabolism. As two hpo-like genes of clusters Nic2-1 and Nic2-2, hpo1, and hpo2 also showed additive effect on the nicotine degrading, but hpo1 provided more contribution than hpo2. The third hpo-like gene in cluster NA (nicotinic acid degrading), nicX is not necessary for 2,5-dihydroxypyridine transformation when hpo1 and hpo2 exist. A variety of transposases and integrases observed around Nic1 and Nic2 cluster genes suggests that the duplicated genes could evolve from horizontal gene transfer (HGT)-related dissemination. This study provide an insight into a novel adaptability mechanism of strains in extreme environment such as high nicotine concentration, and potential novel targets to enhance strain synthesis/degradation ability for future applications.

Keywords

Nicotine degradation Synergistic effect Functional module Pseudomonas Tobacco waste extract 

Notes

Acknowledgments

The authors are grateful to Professor Ningyi Zhou and Xuehong Zhang (Shanghai Jiaotong University, China) for kindly supplying plasmids and providing critical suggestion. The authors also thank Jim Spain (Georgia Institute of Technology, USA) for reading the manuscript and suggestion for revision.

Author contributions

JL, MS, and WZ conceived and designed the experiments. JL, JW, SL, FY, MJS, YJ, FT, and CZ performed the experiments. JL, JW, SL, FY, JX, YJ, HZ, and SQ analyzed the data. JL and WZ contributed reagents/materials. JL, JW, and WZ wrote the manuscript.

Funding

This study was supported by the National Natural Science Foundation (31670115, 31800118), and the China Postdoctoral Science Foundation (2017M621965).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2019_9800_MOESM1_ESM.pdf (1.2 mb)
ESM 1 (PDF 1238 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Biotechnology and BioengineeringZhejiang University of TechnologyHangzhouChina
  2. 2.Technology CenterChina Tobacco Zhejiang Industrial Co., Ltd.HangzhouChina
  3. 3.Technology CenterHangzhou Liqun Environmental Protection Paper Co., Ltd.HangzhouChina

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