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Title: Unifying themes and distinct features of carbon and nitrogen assimilation by polysaccharide-degrading bacteria: a summary of four model systems

Abstract

Our current understanding of enzymatic polysaccharide degradation has come from a huge number of in vitro studies with purified enzymes. While this vast body of work has been invaluable in identifying and characterizing novel mechanisms of action and engineering desirable traits into these enzymes, a comprehensive picture of how these enzymes work as part of a native in vivo system is less clear. Recently, several model bacteria have emerged with genetic systems that allow for a more nuanced study of carbohydrate active enzymes (CAZymes) and how their activity affects bacterial carbon metabolism. With these bacterial model systems it is now possible to not only study a single nutrient system in isolation (i.e. carbohydrate degradation and carbon metabolism), but also how multiple systems are integrated. Given that most environmental polysaccharides are carbon rich but nitrogen poor (e.g. lignocellulose), the interplay between carbon and nitrogen metabolism in polysaccharide-degrading bacteria can now be studied in a physiologically relevant manner. Therefore, in this review we have summarized what has been experimentally determined for CAZyme regulation, production, and export in relation to nitrogen metabolism for two Gram-positive (Caldicellulosiruptor bescii and Clostridium thermocellum) and two Gram-negative (Bacteroides thetaiotaomicron and Cellvibrio japonicus) polysaccharide-degrading bacteria. By comparing andmore » contrasting these four bacteria we have highlighted the shared and unique features of each, with a focus on in vivo studies, in regard to carbon and nitrogen assimilation. Finally, we conclude with what we believe are two important questions that can act as guideposts for future work to better understand the integration of carbon and nitrogen metabolism in polysaccharide-degrading bacteria.« less

Authors:
ORCiD logo [1];  [1]
  1. Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States)
Publication Date:
Research Org.:
Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1834062
Grant/Contract Number:  
SC0014183; 0801830
Resource Type:
Accepted Manuscript
Journal Name:
Applied Microbiology and Biotechnology
Additional Journal Information:
Journal Volume: 105; Journal Issue: 21-22; Journal ID: ISSN 0175-7598
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Bacteroides thetaiotaomicron; Caldicellulosiruptor bescii; Carbohydrate active enzyme; Cellvibrio japonicus; Clostridium thermocellum; Nitrogen metabolism; Polysaccharide

Citation Formats

Gardner, Jeffrey G., and Schreier, Harold J. Unifying themes and distinct features of carbon and nitrogen assimilation by polysaccharide-degrading bacteria: a summary of four model systems. United States: N. p., 2021. Web. doi:10.1007/s00253-021-11614-2.
Gardner, Jeffrey G., & Schreier, Harold J. Unifying themes and distinct features of carbon and nitrogen assimilation by polysaccharide-degrading bacteria: a summary of four model systems. United States. https://doi.org/10.1007/s00253-021-11614-2
Gardner, Jeffrey G., and Schreier, Harold J. Wed . "Unifying themes and distinct features of carbon and nitrogen assimilation by polysaccharide-degrading bacteria: a summary of four model systems". United States. https://doi.org/10.1007/s00253-021-11614-2. https://www.osti.gov/servlets/purl/1834062.
@article{osti_1834062,
title = {Unifying themes and distinct features of carbon and nitrogen assimilation by polysaccharide-degrading bacteria: a summary of four model systems},
author = {Gardner, Jeffrey G. and Schreier, Harold J.},
abstractNote = {Our current understanding of enzymatic polysaccharide degradation has come from a huge number of in vitro studies with purified enzymes. While this vast body of work has been invaluable in identifying and characterizing novel mechanisms of action and engineering desirable traits into these enzymes, a comprehensive picture of how these enzymes work as part of a native in vivo system is less clear. Recently, several model bacteria have emerged with genetic systems that allow for a more nuanced study of carbohydrate active enzymes (CAZymes) and how their activity affects bacterial carbon metabolism. With these bacterial model systems it is now possible to not only study a single nutrient system in isolation (i.e. carbohydrate degradation and carbon metabolism), but also how multiple systems are integrated. Given that most environmental polysaccharides are carbon rich but nitrogen poor (e.g. lignocellulose), the interplay between carbon and nitrogen metabolism in polysaccharide-degrading bacteria can now be studied in a physiologically relevant manner. Therefore, in this review we have summarized what has been experimentally determined for CAZyme regulation, production, and export in relation to nitrogen metabolism for two Gram-positive (Caldicellulosiruptor bescii and Clostridium thermocellum) and two Gram-negative (Bacteroides thetaiotaomicron and Cellvibrio japonicus) polysaccharide-degrading bacteria. By comparing and contrasting these four bacteria we have highlighted the shared and unique features of each, with a focus on in vivo studies, in regard to carbon and nitrogen assimilation. Finally, we conclude with what we believe are two important questions that can act as guideposts for future work to better understand the integration of carbon and nitrogen metabolism in polysaccharide-degrading bacteria.},
doi = {10.1007/s00253-021-11614-2},
journal = {Applied Microbiology and Biotechnology},
number = 21-22,
volume = 105,
place = {United States},
year = {Wed Oct 06 00:00:00 EDT 2021},
month = {Wed Oct 06 00:00:00 EDT 2021}
}

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C aldicellulosiruptor saccharolyticus transcriptomes reveal consequences of chemical pretreatment and genetic modification of lignocellulose
journal, March 2017

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  • Microbial Biotechnology, Vol. 10, Issue 6
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TonB-dependent transport by the gut microbiota: novel aspects of an old problem
journal, August 2018


A Genomic View of the Human-Bacteroides thetaiotaomicron Symbiosis
journal, March 2003


Regulation of the Cellulosomal celS (cel48A) Gene of Clostridium thermocellum Is Growth Rate Dependent
journal, May 2003


An ATP Binding Cassette Transporter Mediates the Uptake of α-(1,6)-Linked Dietary Oligosaccharides in Bifidobacterium and Correlates with Competitive Growth on These Substrates
journal, September 2016

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Caldicellulosiruptor bescii Adheres to Polysaccharides via a Type IV Pilin-Dependent Mechanism
journal, April 2020

  • Khan, Asma M. A. M.; Hauk, Valerie J.; Ibrahim, Mena
  • Applied and Environmental Microbiology, Vol. 86, Issue 9
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On the chemical composition and pyrolytic behavior of hybrid poplar energy crops from northern Spain
journal, February 2020


Prioritization of polysaccharide utilization and control of regulator activation in B acteroides thetaiotaomicron: Regulator activation controls prioritization
journal, February 2017

  • Schwalm, Nathan D.; Townsend, Guy E.; Groisman, Eduardo A.
  • Molecular Microbiology, Vol. 104, Issue 1
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Surface Exposure and Packing of Lipoproteins into Outer Membrane Vesicles Are Coupled Processes in Bacteroides
journal, December 2018

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Nitrogen Assimilation and Global Regulation in Escherichia coli
journal, October 2003


Thermal degradation of crab shell biomass, a nitrogen-containing carbon precursor
journal, March 2020

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Studies on the Aerobic Mesophilic Cellulose-decomposing Bacteria [好氣性中温性纎維素醗酵菌に關する研究]
journal, January 1952

  • Ueda, Kiyomoto; Ishikawa, Shichiro; Itami, Turu
  • Journal of the agricultural chemical society of Japan, Vol. 26, Issue 1
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Searching for principles of microbial physiology
journal, September 2020

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Regulation of the Xylan-degrading Apparatus of Cellvibrio japonicus by a Novel Two-component System
journal, October 2008

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  • Journal of Biological Chemistry, Vol. 284, Issue 2
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A scissor blade-like closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system
journal, April 2012

  • Lowe, E. C.; Basle, A.; Czjzek, M.
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Clostridium thermocellum cellulosomal genes are regulated by extracytoplasmic polysaccharides via alternative sigma factors
journal, October 2010

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Learning from microbial strategies for polysaccharide degradation
journal, February 2016

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Metabolic engineering of Clostridium thermocellum for n-butanol production from cellulose
journal, July 2019

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Engineering dual-glycan responsive expression systems for tunable production of heterologous proteins in Bacteroides thetaiotaomicron
journal, November 2019


Metabolic costs of amino acid and protein production in Escherichia coli
journal, July 2013

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Dynamic responses of B acteroides thetaiotaomicron during growth on glycan mixtures
journal, May 2013

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  • Molecular Microbiology, Vol. 88, Issue 5
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Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria
journal, February 2020


Requirement of the Type II Secretion System for Utilization of Cellulosic Substrates by Cellvibrio japonicus
journal, June 2010

  • Gardner, J. G.; Keating, D. H.
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Comparative Biochemical and Structural Analysis of Novel Cellulose Binding Proteins (Tāpirins) from Extremely Thermophilic Caldicellulosiruptor Species
journal, February 2019

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Three cellulosomal xylanase genes in Clostridium thermocellum are regulated by both vegetative SigA (σ A ) and alternative SigI6 (σ I6 ) factors
journal, August 2015


Biochemical and Mutational Analyses of a Multidomain Cellulase/Mannanase from Caldicellulosiruptor bescii
journal, January 2012

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If You Eat It or Secrete It, They Will Grow: the Expanding List of Nutrients Utilized by Human Gut Bacteria
journal, April 2021

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Comparative genomics and evolution of regulons of the LacI-family transcription factors
journal, June 2014

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Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation
journal, January 2011

  • Raman, Babu; McKeown, Catherine K; Rodriguez, Miguel
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Bacterial α-diglucoside metabolism: perspectives and potential for biotechnology and biomedicine
journal, May 2021

  • Garcia, Cecelia A.; Gardner, Jeffrey G.
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Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013

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