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Title: Efficient chito–oligosaccharide utilization requires two TonB–dependent transporters and one hexosaminidase in Cellvibrio japonicus

Abstract

Abstract Chitin utilization by microbes plays a significant role in biosphere carbon and nitrogen cycling, and studying the microbial approaches used to degrade chitin will facilitate our understanding of bacterial strategies to degrade a broad range of recalcitrant polysaccharides. The early stages of chitin depolymerization by the bacterium  Cellvibrio japonicus  have been characterized and are dependent on one chitin‐specific lytic polysaccharide monooxygenase and nonredundant glycoside hydrolases from the family GH18 to generate chito‐oligosaccharides for entry into metabolism. Here, we describe the mechanisms for the latter stages of chitin utilization by C. japonicus with an emphasis on the fate of chito‐oligosaccharides. Our systems biology approach combined transcriptomics and bacterial genetics using ecologically relevant substrates to determine the essential mechanisms for chito‐oligosaccharide transport and catabolism in C. japonicus . Using RNAseq analysis we found a coordinated expression of genes that encode polysaccharide‐degrading enzymes. Mutational analysis determined that the hex20B gene product, predicted to encode a hexosaminidase, was required for efficient utilization of chito‐oligosaccharides. Furthermore, two gene loci (CJA_0353 and CJA_1157), which encode putative TonB‐dependent transporters, were also essential for chito‐oligosaccharides utilization. This study further develops our model of C. japonicus  chitin metabolism and may be predictive for other environmentally or industrially importantmore » bacteria.« less

Authors:
 [1]; ORCiD logo [1]
  1. Univ. of Maryland - Baltimore County, MD (United States)
Publication Date:
Research Org.:
Univ. of Maryland - Baltimore County, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1774542
Alternate Identifier(s):
OSTI ID: 1880402
Grant/Contract Number:  
SC0014183
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Microbiology
Additional Journal Information:
Journal Volume: 116; Journal Issue: 2; Journal ID: ISSN 0950-382X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Cellvibrio japonicus; chitin; glycoside hydrolase; hexosaminidase; TonB‐dependent transporter

Citation Formats

Monge, Estela C., and Gardner, Jeffrey G. Efficient chito–oligosaccharide utilization requires two TonB–dependent transporters and one hexosaminidase in Cellvibrio japonicus. United States: N. p., 2021. Web. doi:10.1111/mmi.14717.
Monge, Estela C., & Gardner, Jeffrey G. Efficient chito–oligosaccharide utilization requires two TonB–dependent transporters and one hexosaminidase in Cellvibrio japonicus. United States. https://doi.org/10.1111/mmi.14717
Monge, Estela C., and Gardner, Jeffrey G. Thu . "Efficient chito–oligosaccharide utilization requires two TonB–dependent transporters and one hexosaminidase in Cellvibrio japonicus". United States. https://doi.org/10.1111/mmi.14717. https://www.osti.gov/servlets/purl/1774542.
@article{osti_1774542,
title = {Efficient chito–oligosaccharide utilization requires two TonB–dependent transporters and one hexosaminidase in Cellvibrio japonicus},
author = {Monge, Estela C. and Gardner, Jeffrey G.},
abstractNote = {Abstract Chitin utilization by microbes plays a significant role in biosphere carbon and nitrogen cycling, and studying the microbial approaches used to degrade chitin will facilitate our understanding of bacterial strategies to degrade a broad range of recalcitrant polysaccharides. The early stages of chitin depolymerization by the bacterium  Cellvibrio japonicus  have been characterized and are dependent on one chitin‐specific lytic polysaccharide monooxygenase and nonredundant glycoside hydrolases from the family GH18 to generate chito‐oligosaccharides for entry into metabolism. Here, we describe the mechanisms for the latter stages of chitin utilization by C. japonicus with an emphasis on the fate of chito‐oligosaccharides. Our systems biology approach combined transcriptomics and bacterial genetics using ecologically relevant substrates to determine the essential mechanisms for chito‐oligosaccharide transport and catabolism in C. japonicus . Using RNAseq analysis we found a coordinated expression of genes that encode polysaccharide‐degrading enzymes. Mutational analysis determined that the hex20B gene product, predicted to encode a hexosaminidase, was required for efficient utilization of chito‐oligosaccharides. Furthermore, two gene loci (CJA_0353 and CJA_1157), which encode putative TonB‐dependent transporters, were also essential for chito‐oligosaccharides utilization. This study further develops our model of C. japonicus  chitin metabolism and may be predictive for other environmentally or industrially important bacteria.},
doi = {10.1111/mmi.14717},
journal = {Molecular Microbiology},
number = 2,
volume = 116,
place = {United States},
year = {Thu Mar 18 00:00:00 EDT 2021},
month = {Thu Mar 18 00:00:00 EDT 2021}
}

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