Diauxic growth of Fibrobacter succinogenes S85 on cellobiose and lactose

ABSTRACT Fibrobacter succinogenes rapidly colonizes the preruminant calf rumen and becomes a dominant cellulolytic bacterium in the rumen after weaning. Although F. succinogenes actively degrades cellulose in the rumen, it seems that there is no or little of its substrate, cellulose, in the rumen of preweaned calves. We thus evaluated the ability of F. succinogenes to utilize lactose, a main sugar of milk, with or without the presence of cellobiose. We grew F. succinogenes S85 on media containing 2.5% lactose combined with 0%‐0.2% cellobiose or a medium with 0.2% cellobiose but without lactose. The generation times on the 0.2% cellobiose medium and the 2.5% lactose medium were 1.9 and 16.2 h, respectively. The bacterium showed rapid growth on cellobiose and diauxic growth on the lactose media containing 0.05%‐0.2% cellobiose. Moreover, the production of &bgr;‐galactosidase was low in the presence of 0.1%‐0.2% cellobiose. Since the &bgr;‐galactosidase contained a signal peptide and a Por secretion system C‐terminal sorting domain, we speculate that the &bgr;‐galactosidase would be secreted from the bacterial cells by the Por secretion system. Our data indicate the possibility that F. succinogenes could colonize preruminant calf rumen, consuming the lactose present in cow milk.

[1]  H. C. Mantovani,et al.  The effects of increasing amounts of milk replacer powder added to whole milk on passage rate, nutrient digestibility, ruminal development, and body composition in dairy calves. , 2016, Journal of dairy science.

[2]  M. Steele,et al.  Development of Ruminal and Fecal Microbiomes Are Affected by Weaning But Not Weaning Strategy in Dairy Calves , 2016, Front. Microbiol..

[3]  Lara Bereza-Malcolm,et al.  Uptake of milk with and without solid feed during the monogastric phase: Effect on fibrolytic and methanogenic microorganisms in the gastrointestinal tract of calves. , 2016, Animal science journal = Nihon chikusan Gakkaiho.

[4]  Meagan C. Burnet,et al.  Evaluating Models of Cellulose Degradation by Fibrobacter succinogenes S85 , 2015, PloS one.

[5]  P. Wright,et al.  Influence of Substrates on the Surface Characteristics and Membrane Proteome of Fibrobacter succinogenes S85 , 2015, PloS one.

[6]  L. Guan,et al.  The Gut Microbiome and Its Potential Role in the Development and Function of Newborn Calf Gastrointestinal Tract , 2015, Front. Vet. Sci..

[7]  Lara Bereza-Malcolm,et al.  Presence of Selected Methanogens, Fibrolytic Bacteria, and Proteobacteria in the Gastrointestinal Tract of Neonatal Dairy Calves from Birth to 72 Hours , 2015, PloS one.

[8]  K. Nakayama Porphyromonas gingivalis and related bacteria: from colonial pigmentation to the type IX secretion system and gliding motility , 2014, Journal of periodontal research.

[9]  O. Bouchez,et al.  Establishment of ruminal bacterial community in dairy calves from birth to weaning is sequential , 2014, Journal of applied microbiology.

[10]  L. Guan,et al.  Taxonomic Identification of Commensal Bacteria Associated with the Mucosa and Digesta throughout the Gastrointestinal Tracts of Preweaned Calves , 2014, Applied and Environmental Microbiology.

[11]  Cristina González-Fernández,et al.  Enhancing methane production of Chlorella vulgaris via thermochemical pretreatments. , 2013, Bioresource technology.

[12]  I. Mizrahi,et al.  Exploring the bovine rumen bacterial community from birth to adulthood , 2013, The ISME Journal.

[13]  M. McBride,et al.  Gliding Motility and Por Secretion System Genes Are Widespread among Members of the Phylum Bacteroidetes , 2012, Journal of bacteriology.

[14]  Robert W. Li,et al.  The Bacterial Community Composition of the Bovine Rumen Detected Using Pyrosequencing of 16S rRNA Genes , 2012 .

[15]  Qunfeng Dong,et al.  Evaluation of the RDP Classifier Accuracy Using 16S rRNA Gene Variable Regions , 2012 .

[16]  P. Brandt The bacterial community of marine copepods , 2011 .

[17]  Ekaterina Mostovenko,et al.  Protein expression dynamics during Escherichia Coli glucose-lactose diauxie , 2011, BMC Microbiology.

[18]  Natalia N. Ivanova,et al.  The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist , 2011, PloS one.

[19]  R. Mackie,et al.  Biochemical and Domain Analyses of FSUAxe6B, a Modular Acetyl Xylan Esterase, Identify a Unique Carbohydrate Binding Module in Fibrobacter succinogenes S85 , 2009, Journal of bacteriology.

[20]  P. Weimer,et al.  Quantitative analysis of cellulose degradation and growth of cellulolytic bacteria in the rumen. , 2009, FEMS microbiology ecology.

[21]  A. Delort,et al.  Production of oligosaccharides and cellobionic acid by Fibrobacter succinogenes S85 growing on sugars, cellulose and wheat straw , 2009, Applied Microbiology and Biotechnology.

[22]  A. Toyoda,et al.  Isolation and Identification of Cellulose-Binding Proteins from Sheep Rumen Contents , 2009, Applied and Environmental Microbiology.

[23]  S. Koike,et al.  Fibrolytic Rumen Bacteria: Their Ecology and Functions , 2009 .

[24]  S. Koike,et al.  Ecological and physiological characterization shows that Fibrobacter succinogenes is important in rumen fiber digestion — Review , 2008, Folia Microbiologica.

[25]  B. Jayarao,et al.  A survey of bovine colostrum composition and colostrum management practices on Pennsylvania dairy farms. , 2007, Journal of dairy science.

[26]  J. Gong,et al.  Outer Membrane Proteins of Fibrobacter succinogenes with Potential Roles in Adhesion to Cellulose and in Cellulose Digestion , 2007, Journal of bacteriology.

[27]  H. Taniyama,et al.  Expression and distribution of monocarboxylate transporter 1 (MCT1) in the gastrointestinal tract of calves. , 2005, Research in veterinary science.

[28]  J. Russell,et al.  The Effect of Cellobiose, Glucose, and Cellulose on the Survival of Fibrobacter succinogenes A3C Cultures Grown Under Ammonia Limitation , 2004, Current Microbiology.

[29]  I. S. Pretorius,et al.  Microbial Cellulose Utilization: Fundamentals and Biotechnology , 2002, Microbiology and Molecular Biology Reviews.

[30]  Kevin L. Griffith,et al.  Measuring beta-galactosidase activity in bacteria: cell growth, permeabilization, and enzyme assays in 96-well arrays. , 2002, Biochemical and biophysical research communications.

[31]  C. Forsberg,et al.  A Cold-Active Glucanase from the Ruminal BacteriumFibrobacter succinogenes S85 , 1999, Applied and Environmental Microbiology.

[32]  T. Egli,et al.  Growth Kinetics of Suspended Microbial Cells: From Single-Substrate-Controlled Growth to Mixed-Substrate Kinetics , 1998, Microbiology and Molecular Biology Reviews.

[33]  A. Delort,et al.  13C and 1H Nuclear Magnetic Resonance Study of Glycogen Futile Cycling in Strains of the Genus Fibrobacter , 1998, Applied and Environmental Microbiology.

[34]  H. Flint,et al.  The rumen microbial ecosystem--some recent developments. , 1997, Trends in microbiology.

[35]  B. Jesse,et al.  Effect of volatile fatty acid infusion on development of the rumen epithelium in neonatal sheep. , 1997, Journal of dairy science.

[36]  J. Wells,et al.  Why do many ruminal bacteria die and lyse so quickly? , 1996, Journal of dairy science.

[37]  P. Weimer Why don't ruminal bacteria digest cellulose faster? , 1996, Journal of dairy science.

[38]  J. Gong,et al.  Cellulose-binding proteins of Fibrobacter succinogenes and the possible role of a 180-kDa cellulose-binding glycoprotein in adhesion to cellulose , 1996 .

[39]  G. Jones,et al.  Microbial attachment and feed digestion in the rumen. , 1994, Journal of animal science.

[40]  T. L. Glass,et al.  Cellobiose uptake by the cellulolytic ruminal anaerobe Fibrobacter (Bacteroides) succinogenes. , 1991, Canadian journal of microbiology.

[41]  A. M. Gibbins,et al.  Extracellular beta-galactosidase activity of a Fibrobacter succinogenes S85 mutant able to catabolize lactose , 1990, Applied and environmental microbiology.

[42]  D. Stahl,et al.  Transfer of Bacteroides succinogenes (Hungate) to Fibrobacter gen. nov. as Fibrobacter succinogenes comb. nov. and Description of Fibrobacter intestinalis sp. nov. , 1988 .

[43]  C. Franklund,et al.  Glucose uptake by the cellulolytic ruminal anaerobe Bacteroides succinogenes , 1987, Journal of bacteriology.

[44]  M. P. Bryant,et al.  A Study of Actively Cellulolytic Rod-Shaped Bacteria of the Bovine Rumen , 1954 .

[45]  Robert W. Li,et al.  Characterization of the rumen microbiota of pre-ruminant calves using metagenomic tools. , 2012, Environmental microbiology.

[46]  P. Weimer,et al.  Competition among three predominant ruminal cellulolytic bacteria in the absence or presence of non-cellulolytic bacteria. , 2001, Microbiology.

[47]  T. McAllister,et al.  Compartmentation in the rumen , 1997 .

[48]  M. Mitsumori,et al.  Presence of several cellulose-binding proteins in cell lysate of Fibrobacter succinogenes S85 , 1993 .

[49]  M. Otsuka,et al.  COLONIZATION OF MICROORGANISMS IN THE RUMEN OF YOUNG CALVES , 1992 .

[50]  K. Cheng,et al.  [Use of glucose and cellobiose by 3 strains of Fibrobacter succinogenes]. , 1990, Reproduction, nutrition, development.

[51]  G. Gaudet,et al.  Utilisation du glucose et du cellobiose par trois souches de Fibrobacter succinogenes , 1990 .

[52]  T. Hamaoka,et al.  CELLULAR FATTY ACID AND SUGAR COMPOSITION OF REPRESENTATIVE STRAINS OF RUMEN BACTERIA , 1988 .