DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Streptococcus mutans Displays Altered Stress Responses While Enhancing Biofilm Formation by Lactobacillus casei in Mixed-Species Consortium

Abstract

Like Streptococcus mutans, lactobacilli are commonly isolated from carious sites, although their exact role in caries development remains unclear. This study used mixed-species models to analyze biofilm formation by major groups of oral lactobacilli, including L. casei, L. fermentum, L. rhamnosus, L. salivarius ssp. salivarius, and L. gasseri. The results showed that lactobacilli did not form good biofilms when grown alone, although differences existed between different species. When grown together with S. mutans, biofilm formation by L. gasseri and L. rhamnosus was increased by 2-log (P < 0.001), while biofilms by L. fermentum reduced by >1-log (P < 0.001). L. casei enhanced biofilm formation by ~2-log when grown with S. mutans wild-type, but no such effects were observed with S. mutans deficient of glucosyltransferase GtfB and adhesin P1. Both S. mutans and L. casei in dual-species enhanced resistance to acid killing with increases of survival rate by >1-log (P < 0.001), but drastically reduced the survival rates following exposure to hydrogen peroxide (P < 0.001), as compared to the respective mono-species cultures. When analyzed by RNA-seq, more than 134 genes were identified in S. mutans in dual-species with L. casei as either up- or down-regulated when compared to those grownmore » alone. The up-regulated genes include those for superoxide dismutase, NADH oxidase, and members of the mutanobactin biosynthesis cluster. Among the down-regulated genes were those for GtfB and alternative sigma factor SigX. These results further suggest that interactions between S. mutans and oral lactobacilli are species-specific and may have significant impact on cariogenic potential of the community.« less

Authors:
 [1];  [2];  [2];  [3];  [3];  [4];  [3];  [4];  [5];  [6];  [5]
  1. Louisiana State University Health Sciences Center, New Orleans, LA, (United States). Center of Oral and Craniofacial Biology, Dept. of Comprehensive Dentistry and Biomaterials, Dept. of Microbiology, Immunology and Parasitology
  2. Center of Oral and Craniofacial Biology, Louisiana State University Health Sciences Center, New Orleans, LA (United States)
  3. Department of Comprehensive Dentistry and Biomaterials, Louisiana State University Health Sciences Center, New Orleans, LA, (United States)
  4. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Genome Science Group, Bioscience Div.
  5. Basic Science and Craniofacial Biology, New York University College of Dentistry, New York, NY, (United States)
  6. Biofilm Research Labs, Levy Center for Oral Health, Department of Orthodontics, School of Dental Medicine, University of Pennsylvania, Philadelphia, PA, (United States)
Publication Date:
Research Org.:
Los Alamos National Lab (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA); National Institutes of Health (NIH) National Institute of Dental and Craniofacial Research (NIDCR)
OSTI Identifier:
1628034
Grant/Contract Number:  
AC52-06NA25396; DE19452; DE25348
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Cellular and Infection Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2235-2988
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
Immunology; Microbiology

Citation Formats

Wen, Zezhang T., Liao, Sumei, Bitoun, Jacob P., De, Arpan, Jorgensen, Ashton, Feng, Shihai, Xu, Xiaoming, Chain, Patrick S. G., Caufield, Page W., Koo, Hyun, and Li, Yihong. Streptococcus mutans Displays Altered Stress Responses While Enhancing Biofilm Formation by Lactobacillus casei in Mixed-Species Consortium. United States: N. p., 2017. Web. doi:10.3389/fcimb.2017.00524.
Wen, Zezhang T., Liao, Sumei, Bitoun, Jacob P., De, Arpan, Jorgensen, Ashton, Feng, Shihai, Xu, Xiaoming, Chain, Patrick S. G., Caufield, Page W., Koo, Hyun, & Li, Yihong. Streptococcus mutans Displays Altered Stress Responses While Enhancing Biofilm Formation by Lactobacillus casei in Mixed-Species Consortium. United States. https://doi.org/10.3389/fcimb.2017.00524
Wen, Zezhang T., Liao, Sumei, Bitoun, Jacob P., De, Arpan, Jorgensen, Ashton, Feng, Shihai, Xu, Xiaoming, Chain, Patrick S. G., Caufield, Page W., Koo, Hyun, and Li, Yihong. Wed . "Streptococcus mutans Displays Altered Stress Responses While Enhancing Biofilm Formation by Lactobacillus casei in Mixed-Species Consortium". United States. https://doi.org/10.3389/fcimb.2017.00524. https://www.osti.gov/servlets/purl/1628034.
@article{osti_1628034,
title = {Streptococcus mutans Displays Altered Stress Responses While Enhancing Biofilm Formation by Lactobacillus casei in Mixed-Species Consortium},
author = {Wen, Zezhang T. and Liao, Sumei and Bitoun, Jacob P. and De, Arpan and Jorgensen, Ashton and Feng, Shihai and Xu, Xiaoming and Chain, Patrick S. G. and Caufield, Page W. and Koo, Hyun and Li, Yihong},
abstractNote = {Like Streptococcus mutans, lactobacilli are commonly isolated from carious sites, although their exact role in caries development remains unclear. This study used mixed-species models to analyze biofilm formation by major groups of oral lactobacilli, including L. casei, L. fermentum, L. rhamnosus, L. salivarius ssp. salivarius, and L. gasseri. The results showed that lactobacilli did not form good biofilms when grown alone, although differences existed between different species. When grown together with S. mutans, biofilm formation by L. gasseri and L. rhamnosus was increased by 2-log (P < 0.001), while biofilms by L. fermentum reduced by >1-log (P < 0.001). L. casei enhanced biofilm formation by ~2-log when grown with S. mutans wild-type, but no such effects were observed with S. mutans deficient of glucosyltransferase GtfB and adhesin P1. Both S. mutans and L. casei in dual-species enhanced resistance to acid killing with increases of survival rate by >1-log (P < 0.001), but drastically reduced the survival rates following exposure to hydrogen peroxide (P < 0.001), as compared to the respective mono-species cultures. When analyzed by RNA-seq, more than 134 genes were identified in S. mutans in dual-species with L. casei as either up- or down-regulated when compared to those grown alone. The up-regulated genes include those for superoxide dismutase, NADH oxidase, and members of the mutanobactin biosynthesis cluster. Among the down-regulated genes were those for GtfB and alternative sigma factor SigX. These results further suggest that interactions between S. mutans and oral lactobacilli are species-specific and may have significant impact on cariogenic potential of the community.},
doi = {10.3389/fcimb.2017.00524},
journal = {Frontiers in Cellular and Infection Microbiology},
number = ,
volume = 7,
place = {United States},
year = {Wed Dec 20 00:00:00 EST 2017},
month = {Wed Dec 20 00:00:00 EST 2017}
}

Works referenced in this record:

Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen
journal, October 2002

  • Ajdic, D.; McShan, W. M.; McLaughlin, R. E.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 22
  • DOI: 10.1073/pnas.172501299

Ecology of Lactobacilli in the Oral Cavity: A Review of Literature
journal, May 2008


Streptococcus mutans NADH Oxidase Lies at the Intersection of Overlapping Regulons Controlled by Oxygen and NAD+ Levels
journal, March 2014

  • Baker, J. L.; Derr, A. M.; Karuppaiah, K.
  • Journal of Bacteriology, Vol. 196, Issue 12
  • DOI: 10.1128/JB.01542-14

Streptococcus mutans glucan-binding protein-A affects Streptococcus gordonii biofilm architecture
journal, February 2007


Role of a cell surface-associated protein in adherence and dental caries.
journal, January 1991


The changing faces of Streptococcus antigen I/II polypeptide family adhesins: Streptococcus antigen I/II family proteins
journal, May 2010


Oral Streptococci... Products of Their Environment
journal, March 1998


Progress Dissecting the Oral Microbiome in Caries and Health
journal, August 2012


Diversity of Lactobacilli in the Oral Cavities of Young Women with Dental Caries
journal, December 2006

  • Caufield, P. W.; Li, Y.; Dasanayake, A.
  • Caries Research, Vol. 41, Issue 1
  • DOI: 10.1159/000096099

Oral Lactobacilli and Dental Caries: A Model for Niche Adaptation in Humans
journal, March 2015

  • Caufield, P. W.; Schön, C. N.; Saraithong, P.
  • Journal of Dental Research, Vol. 94, Issue 9_suppl
  • DOI: 10.1177/0022034515576052

Identification of a salivary agglutinin-binding domain within cell surface adhesin P1 of Streptococcus mutans.
journal, January 1993


Bacterial GtfB Augments Candida albicans Accumulation in Cross-Kingdom Biofilms
journal, June 2017


Iron requirement of Lactobacillus spp. in completely chemically defined growth media
journal, April 2000


Novel amelogenin-releasing hydrogel for remineralization of enamel artificial caries
journal, September 2012

  • Fan, Yuwei; Wen, Zezhang T.; Liao, Sumei
  • Journal of Bioactive and Compatible Polymers, Vol. 27, Issue 6
  • DOI: 10.1177/0883911512458050

Biofilm growth of Lactobacillus species is promoted by Actinomyces species and Streptococcus mutans
journal, October 2004


Basic Biological Sciences: Cariogenicity of Human Oral Lactobacilli in Hamsters
journal, May 1980

  • Fitzgerald, Robert J.; Fitzgerald, Dorothea B.; Adams, Beatrice O.
  • Journal of Dental Research, Vol. 59, Issue 5
  • DOI: 10.1177/00220345800590051501

Role of Glucosyltransferase B in Interactions of Candida albicans with Streptococcus mutans and with an Experimental Pellicle on Hydroxyapatite Surfaces
journal, July 2011

  • Gregoire, S.; Xiao, J.; Silva, B. B.
  • Applied and Environmental Microbiology, Vol. 77, Issue 18
  • DOI: 10.1128/AEM.05203-11

Beyond Streptococcus mutans: Dental Caries Onset Linked to Multiple Species by 16S rRNA Community Analysis
journal, October 2012


Advances in the microbial etiology and pathogenesis of early childhood caries
journal, February 2016

  • Hajishengallis, E.; Parsaei, Y.; Klein, M. I.
  • Molecular Oral Microbiology, Vol. 32, Issue 1
  • DOI: 10.1111/omi.12152

Biology, immunology, and cariogenicity of Streptococcus mutans.
journal, January 1980


RNA-Seq Reveals Enhanced Sugar Metabolism in Streptococcus mutans Co-cultured with Candida albicans within Mixed-Species Biofilms
journal, June 2017


Acid production by streptococci growing at low pH in a chemostat under anaerobic conditions
journal, October 1992


Differential binding specificities of oral streptococcal antigen I/II family adhesins for human or bacterial ligands: N. S. Jakubovics et al.
journal, January 2005


Beyond the oral microbiome: Oral microbiome
journal, September 2011


Differences between single- and dual-species biofilms of Streptococcus mutans and Veillonella parvula in growth, acidogenicity and susceptibility to chlorhexidine
journal, February 2006


Comprehensive Transcriptome Profiles of Streptococcus mutans UA159 Map Core Streptococcal Competence Genes
journal, April 2016


HISAT: a fast spliced aligner with low memory requirements
journal, March 2015

  • Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3317

Candida albicans stimulates Streptococcus mutans microcolony development via cross-kingdom biofilm-derived metabolites
journal, January 2017

  • Kim, Dongyeop; Sengupta, Arjun; Niepa, Tagbo H. R.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep41332

Proteomics of Porphyromonas gingivalis within a model oral microbial community
journal, January 2009

  • Kuboniwa, Masae; Hendrickson, Erik L.; Xia, Qiangwei
  • BMC Microbiology, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2180-9-98

Streptococcus mutans: a new Gram-positive paradigm?
journal, March 2013

  • Lemos, José A.; Quivey, Robert G.; Koo, Hyun
  • Microbiology, Vol. 159, Issue Pt_3
  • DOI: 10.1099/mic.0.066134-0

Genetic transformation of Veillonella parvula: Veillonellae transformation
journal, July 2011


Rapid evaluation and quality control of next generation sequencing data with FaQCs
journal, November 2014


Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Effect of Veillonella parvula on the antimicrobial resistance and gene expression of Streptococcus mutans grown in a dual-species biofilm
journal, June 2008


The mutacins of Streptococcus mutans: regulation and ecology: Mutacins of Streptococcus mutans
journal, December 2011


Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans
journal, January 2014

  • Moye, Zachary D.; Zeng, Lin; Burne, Robert A.
  • Journal of Oral Microbiology, Vol. 6, Issue 1
  • DOI: 10.3402/jom.v6.24878

A study of bacterial counts (lactobacilli) in saliva related to orthodontic appliances
journal, September 1949


edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009


New convenient defined media for [35S]methionine labelling and proteomic analyses of probiotic lactobacilli
journal, March 2006


Role of Urease Enzymes in Stability of a 10-Species Oral Biofilm Consortium Cultivated in a Constant-Depth Film Fermenter
journal, December 2003


Lactobacillus-mediated interference of mutans streptococci in caries-free vs. caries-active subjects
journal, August 2007

  • Simark-Mattsson, Charlotte; Emilson, Claes-Göran; Håkansson, Eva Grahn
  • European Journal of Oral Sciences, Vol. 115, Issue 4
  • DOI: 10.1111/j.1600-0722.2007.00458.x

Binding Forces of Streptococcus mutans P1 Adhesin
journal, January 2015

  • Sullan, Ruby May A.; Li, James K.; Crowley, Paula J.
  • ACS Nano, Vol. 9, Issue 2
  • DOI: 10.1021/nn5058886

Cross-feeding and interkingdom communication in dual-species biofilms of Streptococcus mutans and Candida albicans
journal, May 2014

  • Sztajer, Helena; Szafranski, Szymon P.; Tomasch, Jürgen
  • The ISME Journal, Vol. 8, Issue 11
  • DOI: 10.1038/ismej.2014.73

Folate overproduction in Lactobacillus plantarum WCFS1 causes methotrexate resistance
journal, August 2009


Functional Genomics Approach to Identifying Genes Required for Biofilm Development by Streptococcus mutans
journal, March 2002


Biofilm formation and virulence expression by Streptococcus mutans are altered when grown in dual-species model
journal, January 2010


The pathogenic persona of community-associated oral streptococci: Pathogenic streptococcal communities
journal, June 2011


Inhibitory effect of Lactobacillus salivarius on Streptococcus mutans biofilm formation
journal, September 2014

  • Wu, C. -C.; Lin, C. -T.; Wu, C. -Y.
  • Molecular Oral Microbiology, Vol. 30, Issue 1
  • DOI: 10.1111/omi.12063

Basic Biological Sciences: The Inhibitory Effect of Hydrolytic Products of Starch on in vitro Colonization by Streptococcus mutans
journal, December 1980


ARS2/MAGL signaling in glioblastoma stem cells promotes self-renewal and M2-like polarization of tumor-associated macrophages
journal, June 2020


Functional Genomics Approach to Identifying Genes Required for Biofilm Development by Streptococcus mutans
journal, January 2003


Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
journal, March 2021


Basic Biological Sciences: Blood and Urine Fluoride Concentrations Associated with Topical Fluoride Applications on Dog Gingiva
journal, August 1981


A study of bacterial counts (lactobacilli) in saliva related to orthodontic appliances
journal, September 1949


Binding Forces of Streptococcus mutans P1 Adhesin
journal, January 2015

  • Sullan, Ruby May A.; Li, James K.; Crowley, Paula J.
  • ACS Nano, Vol. 9, Issue 2
  • DOI: 10.1021/nn5058886

HISAT: a fast spliced aligner with low memory requirements
journal, March 2015

  • Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3317

Targeting redox metabolism: the perfect storm induced by acrylamide poisoning in the brain
journal, January 2020


Candida albicans stimulates Streptococcus mutans microcolony development via cross-kingdom biofilm-derived metabolites
journal, January 2017

  • Kim, Dongyeop; Sengupta, Arjun; Niepa, Tagbo H. R.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep41332

Iron requirement of Lactobacillus spp. in completely chemically defined growth media
journal, April 2000


Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen
journal, October 2002

  • Ajdic, D.; McShan, W. M.; McLaughlin, R. E.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 22
  • DOI: 10.1073/pnas.172501299

Crystal Structure of the C-terminal Region of Streptococcus mutans Antigen I/II and Characterization of Salivary Agglutinin Adherence Domains
journal, April 2011

  • Larson, Matthew R.; Rajashankar, Kanagalaghatta R.; Crowley, Paula J.
  • Journal of Biological Chemistry, Vol. 286, Issue 24
  • DOI: 10.1074/jbc.m111.231100

Biofilm growth of Lactobacillus species is promoted by Actinomyces species and Streptococcus mutans
journal, October 2004


Molecular and biochemical characterizations of human oral lactobacilli as putative probiotic candidates
journal, April 2007


Beyond the oral microbiome: Oral microbiome
journal, September 2011


Streptococcus mutans glucan-binding protein-A affects Streptococcus gordonii biofilm architecture
journal, February 2007


Folate overproduction in Lactobacillus plantarum WCFS1 causes methotrexate resistance
journal, August 2009


Differences between single- and dual-species biofilms of Streptococcus mutans and Veillonella parvula in growth, acidogenicity and susceptibility to chlorhexidine
journal, February 2006


Lactobacillus-mediated interference of mutans streptococci in caries-free vs. caries-active subjects
journal, August 2007

  • Simark-Mattsson, Charlotte; Emilson, Claes-Göran; Håkansson, Eva Grahn
  • European Journal of Oral Sciences, Vol. 115, Issue 4
  • DOI: 10.1111/j.1600-0722.2007.00458.x

Inhibitory effect of Lactobacillus salivarius on Streptococcus mutans biofilm formation
journal, September 2014

  • Wu, C. -C.; Lin, C. -T.; Wu, C. -Y.
  • Molecular Oral Microbiology, Vol. 30, Issue 1
  • DOI: 10.1111/omi.12063

Advances in the microbial etiology and pathogenesis of early childhood caries
journal, February 2016

  • Hajishengallis, E.; Parsaei, Y.; Klein, M. I.
  • Molecular Oral Microbiology, Vol. 32, Issue 1
  • DOI: 10.1111/omi.12152

Environmental Influences on Competitive Hydrogen Peroxide Production in Streptococcus gordonii
journal, May 2011

  • Zheng, Lanyan; Itzek, Andreas; Chen, Zhiyun
  • Applied and Environmental Microbiology, Vol. 77, Issue 13
  • DOI: 10.1128/aem.00309-11

Functional Genomics Approach to Identifying Genes Required for Biofilm Development by Streptococcus mutans
journal, January 2003


Symbiotic Relationship between Streptococcus mutans and Candida albicans Synergizes Virulence of Plaque Biofilms In Vivo
journal, February 2014

  • Falsetta, Megan L.; Klein, Marlise I.; Colonne, Punsiri M.
  • Infection and Immunity, Vol. 82, Issue 5
  • DOI: 10.1128/iai.00087-14

Characteristics of Biofilm Formation by Streptococcus mutans in the Presence of Saliva
journal, July 2008

  • Ahn, Sug-Joon; Ahn, Sang-Joon; Wen, Zezhang T.
  • Infection and Immunity, Vol. 76, Issue 9
  • DOI: 10.1128/iai.00422-08

Growth of several cariogenic strains of oral streptococci in a chemically defined medium.
journal, January 1975


Oral ecology and virulence of Lactobacillus casei and Streptococcus mutans in gnotobiotic rats.
journal, January 1981


Effects of oxygen on pyruvate formate-lyase in situ and sugar metabolism of Streptococcus mutans and Streptococcus sanguis.
journal, January 1985


Ecology of Human Oral Lactobacilli
journal, January 1972


Catabolite Control Protein A Controls Hydrogen Peroxide Production and Cell Death in Streptococcus sanguinis
journal, October 2010

  • Zheng, L.; Chen, Z.; Itzek, A.
  • Journal of Bacteriology, Vol. 193, Issue 2
  • DOI: 10.1128/jb.01131-10

Streptococcus gordonii Biofilm Formation: Identification of Genes that Code for Biofilm Phenotypes
journal, March 2000


Competition and Coexistence between Streptococcus mutans and Streptococcus sanguinis in the Dental Biofilm
journal, October 2005


Influence of BrpA on Critical Virulence Attributes of Streptococcus mutans
journal, April 2006


Interspecies Interactions within Oral Microbial Communities
journal, December 2007

  • Kuramitsu, H. K.; He, X.; Lux, R.
  • Microbiology and Molecular Biology Reviews, Vol. 71, Issue 4
  • DOI: 10.1128/mmbr.00024-07

Biology, immunology, and cariogenicity of Streptococcus mutans
journal, June 1980


Diversity of Lactobacilli in the Oral Cavities of Young Women with Dental Caries
journal, December 2006

  • Caufield, P. W.; Li, Y.; Dasanayake, A.
  • Caries Research, Vol. 41, Issue 1
  • DOI: 10.1159/000096099

Oral Lactobacilli and Dental Caries: A Model for Niche Adaptation in Humans
journal, March 2015

  • Caufield, P. W.; Schön, C. N.; Saraithong, P.
  • Journal of Dental Research, Vol. 94, Issue 9_suppl
  • DOI: 10.1177/0022034515576052

Bacterial GtfB Augments Candida albicans Accumulation in Cross-Kingdom Biofilms
journal, June 2017


Oral Streptococci... Products of Their Environment
journal, March 1998


Biofilm formation and virulence expression by Streptococcus mutans are altered when grown in dual-species model
journal, January 2010


Rapid evaluation and quality control of next generation sequencing data with FaQCs
journal, November 2014


Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Beyond Streptococcus mutans: Dental Caries Onset Linked to Multiple Species by 16S rRNA Community Analysis
journal, October 2012


Ecology of Lactobacilli in the Oral Cavity: A Review of Literature
journal, May 2008


RNA-Seq Reveals Enhanced Sugar Metabolism in Streptococcus mutans Co-cultured with Candida albicans within Mixed-Species Biofilms
journal, June 2017


Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans
journal, January 2014

  • Moye, Zachary D.; Zeng, Lin; Burne, Robert A.
  • Journal of Oral Microbiology, Vol. 6, Issue 1
  • DOI: 10.3402/jom.v6.24878

Works referencing / citing this record:

Lactobacilli spp.: real-time evaluation of biofilm growth
journal, March 2020