Differential Modulation of Saliva-Derived Microcosm Biofilms by Antimicrobial Peptide LL-31 and D-LL-31

Kahena R. Soldati; Yaling Jiang; Bernd W. Brandt; Rob A.M. Exterkate; Mark J. Buijs; Kamran Nazmi; Wendy E. Kaman; Lei Cheng; Floris J. Bikker; Wim Crielaard; Daniela L. Zandim-Barcelos; Dong Mei Deng

doi:10.3390/pathogens12111295

Differential Modulation of Saliva-Derived Microcosm Biofilms by Antimicrobial Peptide LL-31 and D-LL-31

Kahena R. Soldati, Yaling Jiang, Bernd W. Brandt, Rob A.M. Exterkate, Mark J. Buijs, Kamran Nazmi, Wendy E. Kaman, Lei Cheng, Floris J. Bikker, Wim Crielaard, Daniela L. Zandim-Barcelos, Dong Mei Deng^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Microbiome modulation, aiming to restore a health-compatible microbiota, is a novel strategy to treat periodontitis. This study evaluated the modulation effects of antimicrobial peptide LL-31 and its D-enantiomer (D-LL-31) on saliva-derived microcosm biofilms, spiked with or without Porphyromonas gingivalis. To this end, one-day-old biofilms were incubated for 24 h with biofilm medium alone, or medium containing 40 µM LL-31 or D-LL-31, after which biofilms were grown for 5 days. Biofilms were assessed at 1 day and 5 days after intervention for the total viable cell counts, dipeptidyl peptidase IV (DPP4) activity, P. gingivalis amount (by qPCR) and microbial composition (by sequencing). The results showed that D-LL-31, not LL-31, significantly reduced the total viable cell counts, the P. gingivalis amount, and the DPP4 activity of the biofilms spiked with P. gingivalis, but only at 1 day after intervention. In the biofilms spiked with P. gingivalis, D-LL-31 tended to reduce the α-diversity and the compositional shift of the biofilms in time as compared to the control and LL-31 groups. In conclusion, D-LL-31 showed a better performance than LL-31 in biofilm modulation. The biofilm modulation function of the peptides could be impaired when the biofilms were in a severely dysbiotic state.

Original language	English
Article number	1295
Pages (from-to)	1-18
Number of pages	18
Journal	Pathogens
Volume	12
Issue number	11
Early online date	29 Oct 2023
DOIs	https://doi.org/10.3390/pathogens12111295
Publication status	Published - Nov 2023

Bibliographical note

This article belongs to the Special Issue: Opportunistic Oral Pathogens in Oral and Systemic Diseases.

Funding Information:
The authors thank Wendy de Wit and Elly van Deutekom-Mulder for their technical assistance in sample preparation for sequencing. This study was supported by the ACTA Research Institute.

Publisher Copyright:
© 2023 by the authors.

Funding

The authors thank Wendy de Wit and Elly van Deutekom-Mulder for their technical assistance in sample preparation for sequencing. This study was supported by the ACTA Research Institute.

Funders	Funder number
Asia Research Institute

Keywords

16S rRNA gene amplicon sequencing
oral microbiome
periodontitis
Porphyromonas gingivalis
saliva-derived microcosm biofilms

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10.3390/pathogens12111295

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Soldati, K. R., Jiang, Y., Brandt, B. W., Exterkate, R. A. M., Buijs, M. J., Nazmi, K., Kaman, W. E., Cheng, L., Bikker, F. J., Crielaard, W., Zandim-Barcelos, D. L., & Deng, D. M. (2023). Differential Modulation of Saliva-Derived Microcosm Biofilms by Antimicrobial Peptide LL-31 and D-LL-31. Pathogens, 12(11), 1-18. Article 1295. https://doi.org/10.3390/pathogens12111295

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abstract = "Microbiome modulation, aiming to restore a health-compatible microbiota, is a novel strategy to treat periodontitis. This study evaluated the modulation effects of antimicrobial peptide LL-31 and its D-enantiomer (D-LL-31) on saliva-derived microcosm biofilms, spiked with or without Porphyromonas gingivalis. To this end, one-day-old biofilms were incubated for 24 h with biofilm medium alone, or medium containing 40 µM LL-31 or D-LL-31, after which biofilms were grown for 5 days. Biofilms were assessed at 1 day and 5 days after intervention for the total viable cell counts, dipeptidyl peptidase IV (DPP4) activity, P. gingivalis amount (by qPCR) and microbial composition (by sequencing). The results showed that D-LL-31, not LL-31, significantly reduced the total viable cell counts, the P. gingivalis amount, and the DPP4 activity of the biofilms spiked with P. gingivalis, but only at 1 day after intervention. In the biofilms spiked with P. gingivalis, D-LL-31 tended to reduce the α-diversity and the compositional shift of the biofilms in time as compared to the control and LL-31 groups. In conclusion, D-LL-31 showed a better performance than LL-31 in biofilm modulation. The biofilm modulation function of the peptides could be impaired when the biofilms were in a severely dysbiotic state.",

keywords = "16S rRNA gene amplicon sequencing, oral microbiome, periodontitis, Porphyromonas gingivalis, saliva-derived microcosm biofilms",

author = "Soldati, {Kahena R.} and Yaling Jiang and Brandt, {Bernd W.} and Exterkate, {Rob A.M.} and Buijs, {Mark J.} and Kamran Nazmi and Kaman, {Wendy E.} and Lei Cheng and Bikker, {Floris J.} and Wim Crielaard and Zandim-Barcelos, {Daniela L.} and Deng, {Dong Mei}",

note = "This article belongs to the Special Issue: Opportunistic Oral Pathogens in Oral and Systemic Diseases. Funding Information: The authors thank Wendy de Wit and Elly van Deutekom-Mulder for their technical assistance in sample preparation for sequencing. This study was supported by the ACTA Research Institute. Publisher Copyright: {\textcopyright} 2023 by the authors.",

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AU - Jiang, Yaling

AU - Brandt, Bernd W.

AU - Exterkate, Rob A.M.

AU - Buijs, Mark J.

AU - Nazmi, Kamran

AU - Kaman, Wendy E.

AU - Cheng, Lei

AU - Bikker, Floris J.

AU - Crielaard, Wim

AU - Zandim-Barcelos, Daniela L.

AU - Deng, Dong Mei

N1 - This article belongs to the Special Issue: Opportunistic Oral Pathogens in Oral and Systemic Diseases. Funding Information: The authors thank Wendy de Wit and Elly van Deutekom-Mulder for their technical assistance in sample preparation for sequencing. This study was supported by the ACTA Research Institute. Publisher Copyright: © 2023 by the authors.

PY - 2023/11

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N2 - Microbiome modulation, aiming to restore a health-compatible microbiota, is a novel strategy to treat periodontitis. This study evaluated the modulation effects of antimicrobial peptide LL-31 and its D-enantiomer (D-LL-31) on saliva-derived microcosm biofilms, spiked with or without Porphyromonas gingivalis. To this end, one-day-old biofilms were incubated for 24 h with biofilm medium alone, or medium containing 40 µM LL-31 or D-LL-31, after which biofilms were grown for 5 days. Biofilms were assessed at 1 day and 5 days after intervention for the total viable cell counts, dipeptidyl peptidase IV (DPP4) activity, P. gingivalis amount (by qPCR) and microbial composition (by sequencing). The results showed that D-LL-31, not LL-31, significantly reduced the total viable cell counts, the P. gingivalis amount, and the DPP4 activity of the biofilms spiked with P. gingivalis, but only at 1 day after intervention. In the biofilms spiked with P. gingivalis, D-LL-31 tended to reduce the α-diversity and the compositional shift of the biofilms in time as compared to the control and LL-31 groups. In conclusion, D-LL-31 showed a better performance than LL-31 in biofilm modulation. The biofilm modulation function of the peptides could be impaired when the biofilms were in a severely dysbiotic state.

AB - Microbiome modulation, aiming to restore a health-compatible microbiota, is a novel strategy to treat periodontitis. This study evaluated the modulation effects of antimicrobial peptide LL-31 and its D-enantiomer (D-LL-31) on saliva-derived microcosm biofilms, spiked with or without Porphyromonas gingivalis. To this end, one-day-old biofilms were incubated for 24 h with biofilm medium alone, or medium containing 40 µM LL-31 or D-LL-31, after which biofilms were grown for 5 days. Biofilms were assessed at 1 day and 5 days after intervention for the total viable cell counts, dipeptidyl peptidase IV (DPP4) activity, P. gingivalis amount (by qPCR) and microbial composition (by sequencing). The results showed that D-LL-31, not LL-31, significantly reduced the total viable cell counts, the P. gingivalis amount, and the DPP4 activity of the biofilms spiked with P. gingivalis, but only at 1 day after intervention. In the biofilms spiked with P. gingivalis, D-LL-31 tended to reduce the α-diversity and the compositional shift of the biofilms in time as compared to the control and LL-31 groups. In conclusion, D-LL-31 showed a better performance than LL-31 in biofilm modulation. The biofilm modulation function of the peptides could be impaired when the biofilms were in a severely dysbiotic state.

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Differential Modulation of Saliva-Derived Microcosm Biofilms by Antimicrobial Peptide LL-31 and D-LL-31

Abstract

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