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Title: Specialized activities and expression differences for Clostridium thermocellum biofilm and planktonic cells

Journal Article · · Scientific Reports
DOI: https://doi.org/10.1038/srep43583 · OSTI ID:1361314
 [1];  [1];  [1];  [1];  [2];  [2];  [1];  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC) and Biosciences Division
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC) and Chemical Sciences Division

Clostridium thermocellum forms biofilms adherent to lignocellulosic feedstock in a typical continuous cell-monolayer to efficiently break down and uptake cellulose hydrolysates. The sessile cells of biofilms may revert to non-adherent planktonic cells through generation of offspring cells or microenvironment constraints such as limited surface area. These interdependent cell populations co-exist and have different contributions to culture activity and growth. Here, we developed a novel bioreactor design to rapidly harvest sessile and planktonic cell populations for omics studies. In RNA-seq analyses, within 3299 protein coding genes, 59% (or 1958 genes) were differentially expressed with a minimum two-fold change between the two cell populations isolated simultaneously at high culture activity. Furthermore, sessile cells had definitive greater expression of genes involved in catabolism of carbohydrates by glycolysis and pyruvate fermentation, ATP generation by proton gradient, the anabolism of proteins and lipids and cellular functions critical for cell division; planktonic cells had notably higher gene expression for flagellar motility and chemotaxis, cellulosomal cellulases and anchoring scaffoldins, and a range of stress induced homeostasis mechanisms such as oxidative stress protection by antioxidants and flavoprotein co-factors, methionine repair, Fe-S cluster assembly and repair in redox proteins, cell growth control through tRNA thiolation, recovery of damaged DNA by nucleotide excision repair and removal of terminal proteins by proteases. Our knowledge of these cellular adaptations will aid the engineering of industrially relevant strains for consolidated bioprocessing of solid lignocellulosic biomass

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1361314
Journal Information:
Scientific Reports, Journal Name: Scientific Reports Vol. 7; ISSN 2045-2322
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (101)

Clostridium thermocellum ATCC27405 transcriptomic, metabolomic and proteomic profiles after ethanol stress journal January 2012
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
The emergence of Clostridium thermocellum as a high utility candidate for consolidated bioprocessing applications journal August 2014
Elucidating central metabolic redox obstacles hindering ethanol production in Clostridium thermocellum journal November 2015
Atypical Glycolysis in Clostridium thermocellum journal February 2013
Form and Function of Clostridium thermocellum Biofilms journal October 2012
KEGG as a reference resource for gene and protein annotation journal October 2015
From cellulosomes to cellulosomics journal January 2008
Closing the carbon balance for fermentation by Clostridium thermocellum (ATCC 27405) journal January 2012
Clostridium thermocellum DSM 1313 transcriptional responses to redox perturbation journal December 2015
The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading journal October 2014
Pseudomonaschemotaxis journal October 2014
Wood Extractives Promote Cellulase Activity on Cellulosic Substrates journal September 2015
Rubredoxin:Oxygen Oxidoreductase Enhances Survival of Desulfovibrio vulgaris Hildenborough under Microaerophilic Conditions journal August 2006
Kinetics and Relative Importance of Phosphorolytic and Hydrolytic Cleavage of Cellodextrins and Cellobiose in Cell Extracts of Clostridium thermocellum journal March 2004
Measurement and quantification of sessile and planktonic microbial populations during the anaerobic digestion of cellulose journal March 2008
Whole Transcriptome Analysis of Acinetobacter baumannii Assessed by RNA-Sequencing Reveals Different mRNA Expression Profiles in Biofilm Compared to Planktonic Cells journal August 2013
Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation journal January 2011
The Perseus computational platform for comprehensive analysis of (prote)omics data journal June 2016
Proteomic analysis of Clostridium thermocellum core metabolism: relative protein expression profiles and growth phase-dependent changes in protein expression journal January 2012
SpoIIIE strips proteins off the DNA during chromosome translocation journal July 2008
From cellulosomes to cellulosomics journal January 2008
A Bacillus subtilis morphogene cluster that includes spoVE is homologous to the mra region of Escherichia coli journal July 1992
Tracking the cellulolytic activity of Clostridium thermocellum biofilms journal January 2013
Functional mechanics of the ATP-dependent Lon protease- lessons from endogenous protein and synthetic peptide substrates journal May 2008
KEGG as a reference resource for gene and protein annotation journal October 2015
Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities journal February 2016
Signaling-mediated bacterial persister formation journal March 2012
Sulfur Amino Acids Regulate Translational Capacity and Metabolic Homeostasis through Modulation of tRNA Thiolation journal July 2013
Transcriptomic analysis of Clostridium thermocellum Populus hydrolysate-tolerant mutant strain shows increased cellular efficiency in response to Populus hydrolysate compared to the wild type strain journal August 2014
Form and Function of Clostridium thermocellum Biofilms journal October 2012
The surprising diversity of clostridial hydrogenases: a comparative genomic perspective journal April 2010
Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment journal July 2016
Molecular characterization of vulnibactin biosynthesis in Vibrio vulnificus indicates the existence of an alternative siderophore journal January 2014
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture journal March 2021
Clostridium thermocellum transcriptomic profiles after exposure to furfural or heat stress journal January 2013
New insights into the ATP-dependent Clp protease: Escherichia coli and beyond journal May 1999
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases journal November 2013
Closing the carbon balance for fermentation by Clostridium thermocellum (ATCC 27405) journal January 2012
Efficient Spore Synthesis in Bacillus subtilis Depends on the CcdA Protein journal May 2000
Atypical Glycolysis in Clostridium thermocellum journal February 2013
tRNA modifications regulate translation during cellular stress journal October 2014
Hsp70 chaperones: Cellular functions and molecular mechanism journal March 2005
Protein Translocation Across the Bacterial Cytoplasmic Membrane journal June 2008
A Bacillus subtilis morphogene cluster that includes spoVE is homologous to the mra region of Escherichia coli journal July 1992
Biofilms: an emergent form of bacterial life journal August 2016
Extra virgin olive oil improved body weight and insulin sensitivity in high fat diet-induced obese LDLr−/−.Leiden mice without attenuation of steatohepatitis journal April 2021
The identification of four histidine kinases that influence sporulation in Clostridium thermocellum journal August 2014
MyriMatch:  Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis journal February 2007
Wood Extractives Promote Cellulase Activity on Cellulosic Substrates journal September 2015
Development and evaluation of methods to infer biosynthesis and substrate consumption in cultures of cellulolytic microorganisms journal April 2013
Proteomic analysis of Clostridium thermocellum core metabolism: relative protein expression profiles and growth phase-dependent changes in protein expression journal January 2012
Elimination of hydrogenase active site assembly blocks H2 production and increases ethanol yield in Clostridium thermocellum journal January 2015
Comparison of single-molecule sequencing and hybrid approaches for finishing the genome of Clostridium autoethanogenum and analysis of CRISPR systems in industrial relevant Clostridia journal January 2014
Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities journal February 2016
Sulfur Amino Acids Regulate Translational Capacity and Metabolic Homeostasis through Modulation of tRNA Thiolation journal July 2013
Rubredoxin:Oxygen Oxidoreductase Enhances Survival of Desulfovibrio vulgaris Hildenborough under Microaerophilic Conditions journal August 2006
Hsp70 chaperones: Cellular functions and molecular mechanism journal March 2005
Transcriptomic analysis of Clostridium thermocellum Populus hydrolysate-tolerant mutant strain shows increased cellular efficiency in response to Populus hydrolysate compared to the wild type strain journal August 2014
Enzyme-microbe synergy during cellulose hydrolysis by Clostridium thermocellum journal October 2006
Biogenesis and functions of bacterial S-layers journal February 2014
The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading journal October 2014
Enzyme-microbe synergy during cellulose hydrolysis by Clostridium thermocellum journal October 2006
Fe-S Cluster Assembly Pathways in Bacteria journal March 2008
Transcriptomic and proteomic analyses of Desulfovibrio vulgaris biofilms: Carbon and energy flow contribute to the distinct biofilm growth state journal January 2012
Efficient Spore Synthesis in Bacillus subtilis Depends on the CcdA Protein journal May 2000
Biogenesis and functions of bacterial S-layers journal February 2014
Insights into the transcriptome profile of mature biofilm of Salmonella Typhimurium on stainless steels surface journal November 2015
Insights into the transcriptome profile of mature biofilm of Salmonella Typhimurium on stainless steels surface journal November 2015
Indole Affects Biofilm Formation in Bacteria journal October 2010
High Ethanol Titers from Cellulose by Using Metabolically Engineered Thermophilic, Anaerobic Microbes journal September 2011
Comparative transcriptomic analysis of Clostridium acetobutylicum biofilm and planktonic cells journal January 2016
The identification of four histidine kinases that influence sporulation in Clostridium thermocellum journal August 2014
tRNA modifications regulate translation during cellular stress journal October 2014
Thermophilic lignocellulose deconstruction journal May 2014
A Unifying Model for the Role of Polyamines in Bacterial Cell Growth, the Polyamine Modulon journal August 2004
Indole Affects Biofilm Formation in Bacteria journal October 2010
A new perspective on lysogeny: prophages as active regulatory switches of bacteria journal September 2015
Biofilms: an emergent form of bacterial life journal August 2016
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering journal August 2009
Clostridium thermocellum transcriptomic profiles after exposure to furfural or heat stress journal January 2013
The surprising diversity of clostridial hydrogenases: a comparative genomic perspective journal April 2010
Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation journal January 2011
Protein Translocation Across the Bacterial Cytoplasmic Membrane journal June 2008
Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure journal February 2016
Fe-S Cluster Assembly Pathways in Bacteria journal March 2008
Global transcriptome analysis of Clostridium thermocellum ATCC 27405 during growth on dilute acid pretreated Populus and switchgrass journal January 2013
A multifaceted role for polyamines in bacterial pathogens journal April 2008
Transcriptomic and proteomic analyses of Desulfovibrio vulgaris biofilms: Carbon and energy flow contribute to the distinct biofilm growth state journal January 2012
A multifaceted role for polyamines in bacterial pathogens journal April 2008
The emergence of Clostridium thermocellum as a high utility candidate for consolidated bioprocessing applications journal August 2014
Development and evaluation of methods to infer biosynthesis and substrate consumption in cultures of cellulolytic microorganisms journal April 2013
Cellodextrin and Laminaribiose ABC Transporters in Clostridium thermocellum journal October 2008
Elimination of hydrogenase active site assembly blocks H2 production and increases ethanol yield in Clostridium thermocellum journal January 2015
Clostridium thermocellum DSM 1313 transcriptional responses to redox perturbation journal December 2015
Clostridium thermocellum ATCC27405 transcriptomic, metabolomic and proteomic profiles after ethanol stress journal January 2012
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering journal August 2009
Comparative transcriptomic analysis of Clostridium acetobutylicum biofilm and planktonic cells journal January 2016
SpoIIIE strips proteins off the DNA during chromosome translocation journal July 2008
A Unifying Model for the Role of Polyamines in Bacterial Cell Growth, the Polyamine Modulon journal August 2004
High Ethanol Titers from Cellulose by Using Metabolically Engineered Thermophilic, Anaerobic Microbes journal September 2011

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Clostridium thermocellum LL1210 pH homeostasis mechanisms informed by transcriptomics and metabolomics journal April 2018
Cellulosomes localise on the surface of membrane vesicles from the cellulolytic bacterium Clostridium thermocellum journal June 2019
Anaerobic microplate assay for direct microbial conversion of switchgrass and Avicel using Clostridium thermocellum journal November 2017
A global analysis of gene expression in Fibrobacter succinogenes S85 grown on cellulose and soluble sugars at different growth rates journal October 2018