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Enterococcus faecalis antagonizes Pseudomonas aeruginosa growth in polymicrobial biofilms

Casandra Ai Zhu Tan, View ORCID ProfileLing Ning Lam, Goran Biukovic, Eliza Ye-Chen Soh, Xiao Wei Toh, View ORCID ProfileJosé A. Lemos, View ORCID ProfileKimberly A. Kline
doi: https://doi.org/10.1101/2022.01.18.476859
Casandra Ai Zhu Tan
1Singapore Centre for Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Singapore
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Ling Ning Lam
2Department of Oral Biology, University of Florida College of Dentistry, Gainesville, Florida, USA
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Goran Biukovic
1Singapore Centre for Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Singapore
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Eliza Ye-Chen Soh
1Singapore Centre for Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Singapore
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Xiao Wei Toh
1Singapore Centre for Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Singapore
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José A. Lemos
2Department of Oral Biology, University of Florida College of Dentistry, Gainesville, Florida, USA
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Kimberly A. Kline
1Singapore Centre for Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Singapore
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  • For correspondence: kkline@ntu.edu.sg
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ABSTRACT

Enterococcus faecalis is often co-isolated with Pseudomonas aeruginosa in polymicrobial biofilm-associated infections of wounds and the urinary tract. As a defense strategy, the host innately restricts iron availability at infection sites. Despite their co-prevalence, the polymicrobial interactions of these two pathogens in iron- restricted conditions, such as those found in the host, remains unexplored. Here we show that E. faecalis inhibits P. aeruginosa growth within biofilms when iron is restricted. E. faecalis lactate dehydrogenase (ldh1) gives rise to L-lactate production during fermentative growth. We find that E. faecalis ldh1 mutant fails to inhibit P. aeruginosa growth. Additionally, we demonstrate that ldh1 expression is induced in iron-restricted conditions, resulting in increased lactic acid exported and consequently, a reduction in pH. Together, our results suggest that E. faecalis synergistically inhibit P. aeruginosa growth by decreasing environmental pH and L-lactate-mediated iron chelation. Overall, this study highlights that the microenvironment in which the infection occurs is important for understanding its pathophysiology.

IMPORTANCE Many infections are polymicrobial and biofilm-associated in nature. Iron is essential for many metabolic processes and plays an important role in controlling infections, where the host restricts iron as a defense mechanism against invading pathogens. However, polymicrobial interactions between pathogens are underexplored in iron- restricted conditions. Here, we explore the polymicrobial interactions between commonly co-isolated E. faecalis and P. aeruginosa within biofilms. We find that E. faecalis modulates the microenvironment by exporting lactic acid which further chelates already limited iron, and also lowers the environmental pH to antagonize P. aeruginosa growth in iron-restricted conditions. Our findings provide insights into polymicrobial interactions between pathogens in an infection-relevant condition and how manipulating the microenvironment can be taken advantage of to better control infections.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 20, 2022.
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Enterococcus faecalis antagonizes Pseudomonas aeruginosa growth in polymicrobial biofilms
Casandra Ai Zhu Tan, Ling Ning Lam, Goran Biukovic, Eliza Ye-Chen Soh, Xiao Wei Toh, José A. Lemos, Kimberly A. Kline
bioRxiv 2022.01.18.476859; doi: https://doi.org/10.1101/2022.01.18.476859
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Enterococcus faecalis antagonizes Pseudomonas aeruginosa growth in polymicrobial biofilms
Casandra Ai Zhu Tan, Ling Ning Lam, Goran Biukovic, Eliza Ye-Chen Soh, Xiao Wei Toh, José A. Lemos, Kimberly A. Kline
bioRxiv 2022.01.18.476859; doi: https://doi.org/10.1101/2022.01.18.476859

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