Polyphosphate-accumulating bacteria: Potential contributors to mineral dissolution in the oral cavity

Ashley A. Breiland; Beverly E. Flood; Julia Nikrad; John Bakarich; Matthew Husman; Taek Hyun Rhee; Robert S. Jones; Jake V. Bailey

doi:10.1128/AEM.02440-17

Polyphosphate-accumulating bacteria: Potential contributors to mineral dissolution in the oral cavity

Ashley A. Breiland, Beverly E. Flood, Julia Nikrad, John Bakarich, Matthew Husman, Taek Hyun Rhee, Robert S. Jones, Jake V. Bailey

Research output: Contribution to journal › Article › peer-review

15 Scopus citations

Abstract

Bacteria that accumulate polyphosphates have previously been shown to dynamically influence the solubility of phosphatic minerals in marine settings and wastewater. Here, we show that dental plaque, saliva, and carious lesions all contain abundant polyphosphate-accumulating bacteria. Saturation state modeling results, informed by phosphate uptake experiments using the model organism Lactobacillus rhamnosus, which is known to inhabit advanced carious lesions, suggest that polyphosphate accumulation can lead to undersaturated conditions with respect to hydroxyapatite under some oral cavity conditions. The cell densities of polyphosphate-accumulating bacteria we observed in some regions of oral biofilms are comparable to those that produce undersaturated conditions (i.e., those that thermodynamically favor mineral dissolution) in our phosphate uptake experiments with L. rhamnosus. These results suggest that the localized generation of undersaturated conditions by polyphosphate- accumulating bacteria constitutes a new potential mechanism of tooth dissolution that may augment the effects of metabolic acid production.

Original language	English (US)
Article number	e02440-17
Journal	Applied and environmental microbiology
Volume	84
Issue number	7
DOIs	https://doi.org/10.1128/AEM.02440-17
State	Published - Apr 1 2018

Bibliographical note

Funding Information:
We thank Chris Crosby, Thomas Pengo, Dan Jones, Mark Sanders, and Guillermo Marques for training, advice, and assistance. Image acquisition and analysis support was provided by the University of Minnesota Imaging Center. We thank the two anonymous reviewers for their comments that greatly improved the manuscript. Funding for this work was provided by the University of Minnesota Office of the Vice President for Research Minnesota Futures Grant Program. J.V.B., B.E.F., and R.S.J. conceived the study and designed the research with input from A.A.B. Experimental data were generated by A.A.B. with help from J.N. Sample collection was conducted by J.B., M.H., T.R., and R.S.J. Genome research and analysis were conducted by B.E.F. A.A.B. and J.V.B. wrote the paper with input from other authors

Publisher Copyright:
© 2018 American Society for Microbiology.

Keywords

Dental caries
Oral biofilms
Polyphosphate

Access

10.1128/AEM.02440-17

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5861820

OpenUrl availability

Full text

Cite this

@article{1a28f722d6e94b8ab9d0df1950ec7b7e,

title = "Polyphosphate-accumulating bacteria: Potential contributors to mineral dissolution in the oral cavity",

abstract = "Bacteria that accumulate polyphosphates have previously been shown to dynamically influence the solubility of phosphatic minerals in marine settings and wastewater. Here, we show that dental plaque, saliva, and carious lesions all contain abundant polyphosphate-accumulating bacteria. Saturation state modeling results, informed by phosphate uptake experiments using the model organism Lactobacillus rhamnosus, which is known to inhabit advanced carious lesions, suggest that polyphosphate accumulation can lead to undersaturated conditions with respect to hydroxyapatite under some oral cavity conditions. The cell densities of polyphosphate-accumulating bacteria we observed in some regions of oral biofilms are comparable to those that produce undersaturated conditions (i.e., those that thermodynamically favor mineral dissolution) in our phosphate uptake experiments with L. rhamnosus. These results suggest that the localized generation of undersaturated conditions by polyphosphate- accumulating bacteria constitutes a new potential mechanism of tooth dissolution that may augment the effects of metabolic acid production.",

keywords = "Dental caries, Oral biofilms, Polyphosphate",

author = "Breiland, {Ashley A.} and Flood, {Beverly E.} and Julia Nikrad and John Bakarich and Matthew Husman and Rhee, {Taek Hyun} and Jones, {Robert S.} and Bailey, {Jake V.}",

note = "Funding Information: We thank Chris Crosby, Thomas Pengo, Dan Jones, Mark Sanders, and Guillermo Marques for training, advice, and assistance. Image acquisition and analysis support was provided by the University of Minnesota Imaging Center. We thank the two anonymous reviewers for their comments that greatly improved the manuscript. Funding for this work was provided by the University of Minnesota Office of the Vice President for Research Minnesota Futures Grant Program. J.V.B., B.E.F., and R.S.J. conceived the study and designed the research with input from A.A.B. Experimental data were generated by A.A.B. with help from J.N. Sample collection was conducted by J.B., M.H., T.R., and R.S.J. Genome research and analysis were conducted by B.E.F. A.A.B. and J.V.B. wrote the paper with input from other authors Publisher Copyright: {\textcopyright} 2018 American Society for Microbiology.",

year = "2018",

month = apr,

day = "1",

doi = "10.1128/AEM.02440-17",

language = "English (US)",

volume = "84",

journal = "Applied and environmental microbiology",

issn = "0099-2240",

publisher = "American Society for Microbiology",

number = "7",

}

TY - JOUR

T1 - Polyphosphate-accumulating bacteria

T2 - Potential contributors to mineral dissolution in the oral cavity

AU - Breiland, Ashley A.

AU - Flood, Beverly E.

AU - Nikrad, Julia

AU - Bakarich, John

AU - Husman, Matthew

AU - Rhee, Taek Hyun

AU - Jones, Robert S.

AU - Bailey, Jake V.

N1 - Funding Information: We thank Chris Crosby, Thomas Pengo, Dan Jones, Mark Sanders, and Guillermo Marques for training, advice, and assistance. Image acquisition and analysis support was provided by the University of Minnesota Imaging Center. We thank the two anonymous reviewers for their comments that greatly improved the manuscript. Funding for this work was provided by the University of Minnesota Office of the Vice President for Research Minnesota Futures Grant Program. J.V.B., B.E.F., and R.S.J. conceived the study and designed the research with input from A.A.B. Experimental data were generated by A.A.B. with help from J.N. Sample collection was conducted by J.B., M.H., T.R., and R.S.J. Genome research and analysis were conducted by B.E.F. A.A.B. and J.V.B. wrote the paper with input from other authors Publisher Copyright: © 2018 American Society for Microbiology.

PY - 2018/4/1

Y1 - 2018/4/1

N2 - Bacteria that accumulate polyphosphates have previously been shown to dynamically influence the solubility of phosphatic minerals in marine settings and wastewater. Here, we show that dental plaque, saliva, and carious lesions all contain abundant polyphosphate-accumulating bacteria. Saturation state modeling results, informed by phosphate uptake experiments using the model organism Lactobacillus rhamnosus, which is known to inhabit advanced carious lesions, suggest that polyphosphate accumulation can lead to undersaturated conditions with respect to hydroxyapatite under some oral cavity conditions. The cell densities of polyphosphate-accumulating bacteria we observed in some regions of oral biofilms are comparable to those that produce undersaturated conditions (i.e., those that thermodynamically favor mineral dissolution) in our phosphate uptake experiments with L. rhamnosus. These results suggest that the localized generation of undersaturated conditions by polyphosphate- accumulating bacteria constitutes a new potential mechanism of tooth dissolution that may augment the effects of metabolic acid production.

AB - Bacteria that accumulate polyphosphates have previously been shown to dynamically influence the solubility of phosphatic minerals in marine settings and wastewater. Here, we show that dental plaque, saliva, and carious lesions all contain abundant polyphosphate-accumulating bacteria. Saturation state modeling results, informed by phosphate uptake experiments using the model organism Lactobacillus rhamnosus, which is known to inhabit advanced carious lesions, suggest that polyphosphate accumulation can lead to undersaturated conditions with respect to hydroxyapatite under some oral cavity conditions. The cell densities of polyphosphate-accumulating bacteria we observed in some regions of oral biofilms are comparable to those that produce undersaturated conditions (i.e., those that thermodynamically favor mineral dissolution) in our phosphate uptake experiments with L. rhamnosus. These results suggest that the localized generation of undersaturated conditions by polyphosphate- accumulating bacteria constitutes a new potential mechanism of tooth dissolution that may augment the effects of metabolic acid production.

KW - Dental caries

KW - Oral biofilms

KW - Polyphosphate

UR - http://www.scopus.com/inward/record.url?scp=85044134975&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85044134975&partnerID=8YFLogxK

U2 - 10.1128/AEM.02440-17

DO - 10.1128/AEM.02440-17

M3 - Article

C2 - 29352083

AN - SCOPUS:85044134975

SN - 0099-2240

VL - 84

JO - Applied and environmental microbiology

JF - Applied and environmental microbiology

IS - 7

M1 - e02440-17

ER -

Polyphosphate-accumulating bacteria: Potential contributors to mineral dissolution in the oral cavity

Abstract

Bibliographical note

Keywords

Access

OpenUrl availability

Other files and links

Fingerprint

Cite this