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Applied and Environmental Microbiology
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Environmental Microbiology

Systematic Analysis of Escherichia coli Isolates from Sheep and Cattle Suggests Adaption to the Rumen Niche

Jian Pang, Zhanying Liu, Qiancheng Zhang, Xuemei Lu, Qingsheng Qi
Shuang-Jiang Liu, Editor
Jian Pang
aSchool of Chemical Engineering, Inner Mongolia University of Technology, Hohhot, China
bState Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
cInner Mongolia Energy Conservation and Emission Reduction Engineering Research Center in Fermentation Industry, Hohhot, China
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Zhanying Liu
aSchool of Chemical Engineering, Inner Mongolia University of Technology, Hohhot, China
cInner Mongolia Energy Conservation and Emission Reduction Engineering Research Center in Fermentation Industry, Hohhot, China
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Qiancheng Zhang
aSchool of Chemical Engineering, Inner Mongolia University of Technology, Hohhot, China
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Xuemei Lu
bState Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
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Qingsheng Qi
bState Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
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Shuang-Jiang Liu
Chinese Academy of Sciences
Roles: Editor
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DOI: 10.1128/AEM.01417-20
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ABSTRACT

The commonly used laboratory bacterium Escherichia coli normally does not produce and secrete cellulases due to its complex bilayer membrane structure and poor secretory apparatus. In our previous study, the cellulolytic E. coli strain ZH-4 with extracellular cellulase activity was found in the bovine rumen. In this study, we demonstrate that the secretion of cellulase is a common feature of E. coli isolates from the rumen of animals such as sheep and cattle. Physiological phenotype characterization of these E. coli isolates, together with genome, transcriptome, and comparative genomics analysis, suggests their adaption to the rumen niche. The higher growth rate of the isolated strains under aerobic conditions meets the competitive requirements of the strains in rumen microecosystem, while anaerobic accumulation of reduced H2 and succinate is hypothesized to be the results of adaptation to the rumen environment. Cellulase secretion increased significantly when the molecular chaperone genes ibpA and ibpB were overexpressed. This was also revealed by the transcriptomic data. A possible mechanism for cellulase secretion by E. coli isolates was proposed based on the transcriptomic data and molecular experiments.

IMPORTANCE As an important intestinal microorganism, E. coli is present in the intestinal tract of animals and in many other environments. However, it normally does not produce and secret cellulases due to its complex bilayer membrane structure and poor secretory apparatus. Here, we proved that E. coli is widely present in the rumen of sheep and cattle. Systematic analysis of the isolates indicated that they have adapted to the rumen niche, with phenotypes that include secretion of cellulase and fermentative accumulation of succinate and H2. The finding that overexpression of small heat shock protein genes ibpA and ibpB could facilitate cellulase BcsZ secretion, which provides a possible insight into the protein secretion mechanism of rumen-colonizing E. coli.

FOOTNOTES

    • Received 15 June 2020.
    • Accepted 3 August 2020.
    • Accepted manuscript posted online 14 August 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Systematic Analysis of Escherichia coli Isolates from Sheep and Cattle Suggests Adaption to the Rumen Niche
Jian Pang, Zhanying Liu, Qiancheng Zhang, Xuemei Lu, Qingsheng Qi
Applied and Environmental Microbiology Oct 2020, 86 (20) e01417-20; DOI: 10.1128/AEM.01417-20

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Systematic Analysis of Escherichia coli Isolates from Sheep and Cattle Suggests Adaption to the Rumen Niche
Jian Pang, Zhanying Liu, Qiancheng Zhang, Xuemei Lu, Qingsheng Qi
Applied and Environmental Microbiology Oct 2020, 86 (20) e01417-20; DOI: 10.1128/AEM.01417-20
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KEYWORDS

Escherichia coli
rumen
BcsZ
molecular chaperone
secretion

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