Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA

Nadia Rostami; Robert C Shields; Hannah J Serrage; Catherine Lawler; Jane L Brittan; Sufian Yassin; Halah Ahmed; Achim Treumann; Paul Thompson; Kevin J Waldron; Angela H Nobbs; Nicholas S Jakubovics

doi:10.1038/s41522-022-00359-z

Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA

Nadia Rostami, Robert C Shields, Hannah J Serrage, Catherine Lawler, Jane L Brittan, Sufian Yassin, Halah Ahmed, Achim Treumann, Paul Thompson, Kevin J Waldron, Angela H Nobbs, Nicholas S Jakubovics^*

^*Corresponding author for this work

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Abstract

Extracellular DNA (eDNA) is a key component of many microbial biofilms including dental plaque. However, the roles of extracellular deoxyribonuclease (DNase) enzymes within biofilms are poorly understood. Streptococcus gordonii is a pioneer colonizer of dental plaque. Here, we identified and characterised SsnA, a cell wall-associated protein responsible for extracellular DNase activity of S. gordonii. The SsnA-mediated extracellular DNase activity of S. gordonii was suppressed following growth in sugars. SsnA was purified as a recombinant protein and shown to be inactive below pH 6.5. SsnA inhibited biofilm formation by Streptococcus mutans in a pH-dependent manner. Further, SsnA inhibited the growth of oral microcosm biofilms in human saliva. However, inhibition was ameliorated by the addition of sucrose. Together, these data indicate that S. gordonii SsnA plays a key role in interspecies competition within oral biofilms. Acidification of the medium through sugar catabolism could be a strategy for cariogenic species such as S. mutans to prevent SsnA-mediated exclusion from biofilms.

Original language	English
Article number	96
Journal	npj Biofilms and Microbiomes
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41522-022-00359-z
Publication status	Published - 12 Dec 2022

Bibliographical note

Funding Information:
This work was funded by an International Association for Dental Research (IADR) Innovation in Oral Care Award (NSJ) and by The Dunhill Medical Trust (RPGF1810\101) (NSJ/AHN/KJW). KJW was funded by the Biotechnology and Biological Sciences Research Council (BB/S006818/1). PhD funding for CL was from the National Institutes of Health (DE016690). We thank Ekaterina Kozhevnikova and Philip Hardy for technical support and the Newcastle University Protein and Proteome Analysis (NUPPA) Core Facility for their assistance in enzyme purification.

Funding Information:
This work was funded by an International Association for Dental Research (IADR) Innovation in Oral Care Award (NSJ) and by The Dunhill Medical Trust (RPGF1810\101) (NSJ/AHN/KJW). KJW was funded by the Biotechnology and Biological Sciences Research Council (BB/S006818/1). PhD funding for CL was from the National Institutes of Health (DE016690). We thank Ekaterina Kozhevnikova and Philip Hardy for technical support and the Newcastle University Protein and Proteome Analysis (NUPPA) Core Facility for their assistance in enzyme purification.

Publisher Copyright:
© 2022, The Author(s).

Keywords

Humans
Streptococcus gordonii/genetics
Dental Plaque
Streptococcus mutans
Biofilms
Saliva

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Rostami, N., Shields, R. C., Serrage, H. J., Lawler, C., Brittan, J. L., Yassin, S., Ahmed, H., Treumann, A., Thompson, P., Waldron, K. J., Nobbs, A. H., & Jakubovics, N. S. (2022). Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA. npj Biofilms and Microbiomes, 8(1), Article 96. https://doi.org/10.1038/s41522-022-00359-z

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abstract = "Extracellular DNA (eDNA) is a key component of many microbial biofilms including dental plaque. However, the roles of extracellular deoxyribonuclease (DNase) enzymes within biofilms are poorly understood. Streptococcus gordonii is a pioneer colonizer of dental plaque. Here, we identified and characterised SsnA, a cell wall-associated protein responsible for extracellular DNase activity of S. gordonii. The SsnA-mediated extracellular DNase activity of S. gordonii was suppressed following growth in sugars. SsnA was purified as a recombinant protein and shown to be inactive below pH 6.5. SsnA inhibited biofilm formation by Streptococcus mutans in a pH-dependent manner. Further, SsnA inhibited the growth of oral microcosm biofilms in human saliva. However, inhibition was ameliorated by the addition of sucrose. Together, these data indicate that S. gordonii SsnA plays a key role in interspecies competition within oral biofilms. Acidification of the medium through sugar catabolism could be a strategy for cariogenic species such as S. mutans to prevent SsnA-mediated exclusion from biofilms.",

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note = "Funding Information: This work was funded by an International Association for Dental Research (IADR) Innovation in Oral Care Award (NSJ) and by The Dunhill Medical Trust (RPGF1810\101) (NSJ/AHN/KJW). KJW was funded by the Biotechnology and Biological Sciences Research Council (BB/S006818/1). PhD funding for CL was from the National Institutes of Health (DE016690). We thank Ekaterina Kozhevnikova and Philip Hardy for technical support and the Newcastle University Protein and Proteome Analysis (NUPPA) Core Facility for their assistance in enzyme purification. Funding Information: This work was funded by an International Association for Dental Research (IADR) Innovation in Oral Care Award (NSJ) and by The Dunhill Medical Trust (RPGF1810\101) (NSJ/AHN/KJW). KJW was funded by the Biotechnology and Biological Sciences Research Council (BB/S006818/1). PhD funding for CL was from the National Institutes of Health (DE016690). We thank Ekaterina Kozhevnikova and Philip Hardy for technical support and the Newcastle University Protein and Proteome Analysis (NUPPA) Core Facility for their assistance in enzyme purification. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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AU - Rostami, Nadia

AU - Shields, Robert C

AU - Serrage, Hannah J

AU - Lawler, Catherine

AU - Brittan, Jane L

AU - Yassin, Sufian

AU - Ahmed, Halah

AU - Treumann, Achim

AU - Thompson, Paul

AU - Waldron, Kevin J

AU - Nobbs, Angela H

AU - Jakubovics, Nicholas S

N1 - Funding Information: This work was funded by an International Association for Dental Research (IADR) Innovation in Oral Care Award (NSJ) and by The Dunhill Medical Trust (RPGF1810\101) (NSJ/AHN/KJW). KJW was funded by the Biotechnology and Biological Sciences Research Council (BB/S006818/1). PhD funding for CL was from the National Institutes of Health (DE016690). We thank Ekaterina Kozhevnikova and Philip Hardy for technical support and the Newcastle University Protein and Proteome Analysis (NUPPA) Core Facility for their assistance in enzyme purification. Funding Information: This work was funded by an International Association for Dental Research (IADR) Innovation in Oral Care Award (NSJ) and by The Dunhill Medical Trust (RPGF1810\101) (NSJ/AHN/KJW). KJW was funded by the Biotechnology and Biological Sciences Research Council (BB/S006818/1). PhD funding for CL was from the National Institutes of Health (DE016690). We thank Ekaterina Kozhevnikova and Philip Hardy for technical support and the Newcastle University Protein and Proteome Analysis (NUPPA) Core Facility for their assistance in enzyme purification. Publisher Copyright: © 2022, The Author(s).

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N2 - Extracellular DNA (eDNA) is a key component of many microbial biofilms including dental plaque. However, the roles of extracellular deoxyribonuclease (DNase) enzymes within biofilms are poorly understood. Streptococcus gordonii is a pioneer colonizer of dental plaque. Here, we identified and characterised SsnA, a cell wall-associated protein responsible for extracellular DNase activity of S. gordonii. The SsnA-mediated extracellular DNase activity of S. gordonii was suppressed following growth in sugars. SsnA was purified as a recombinant protein and shown to be inactive below pH 6.5. SsnA inhibited biofilm formation by Streptococcus mutans in a pH-dependent manner. Further, SsnA inhibited the growth of oral microcosm biofilms in human saliva. However, inhibition was ameliorated by the addition of sucrose. Together, these data indicate that S. gordonii SsnA plays a key role in interspecies competition within oral biofilms. Acidification of the medium through sugar catabolism could be a strategy for cariogenic species such as S. mutans to prevent SsnA-mediated exclusion from biofilms.

AB - Extracellular DNA (eDNA) is a key component of many microbial biofilms including dental plaque. However, the roles of extracellular deoxyribonuclease (DNase) enzymes within biofilms are poorly understood. Streptococcus gordonii is a pioneer colonizer of dental plaque. Here, we identified and characterised SsnA, a cell wall-associated protein responsible for extracellular DNase activity of S. gordonii. The SsnA-mediated extracellular DNase activity of S. gordonii was suppressed following growth in sugars. SsnA was purified as a recombinant protein and shown to be inactive below pH 6.5. SsnA inhibited biofilm formation by Streptococcus mutans in a pH-dependent manner. Further, SsnA inhibited the growth of oral microcosm biofilms in human saliva. However, inhibition was ameliorated by the addition of sucrose. Together, these data indicate that S. gordonii SsnA plays a key role in interspecies competition within oral biofilms. Acidification of the medium through sugar catabolism could be a strategy for cariogenic species such as S. mutans to prevent SsnA-mediated exclusion from biofilms.

KW - Humans

KW - Streptococcus gordonii/genetics

KW - Dental Plaque

KW - Streptococcus mutans

KW - Biofilms

KW - Saliva

U2 - 10.1038/s41522-022-00359-z

DO - 10.1038/s41522-022-00359-z

M3 - Article (Academic Journal)

C2 - 36509765

SN - 2055-5008

VL - 8

JO - npj Biofilms and Microbiomes

JF - npj Biofilms and Microbiomes

IS - 1

M1 - 96

ER -

Interspecies competition in oral biofilms mediated by Streptococcus gordonii extracellular deoxyribonuclease SsnA

Abstract

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Keywords

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