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Dynamic interspecies interactions and robustness in a four-species model biofilm
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  • Aurélie Baliarda,
  • Michèle Winkler,
  • Laurent Tournier,
  • Colin Tinsley,
  • Stéphane Aymerich
Aurélie Baliarda
AgroParisTech
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Michèle Winkler
AgroParisTech
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Laurent Tournier
INRAE
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Colin Tinsley
AgroParisTech
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Stéphane Aymerich
INRAE
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Abstract

Interspecific interactions within biofilms determine relative species abundance, growth dynamics, community resilience, and success or failure of invasion by an extraneous organism. However, deciphering interspecific interactions and assessing their contribution to biofilm properties and function remain a challenge. Here, we describe the constitution of a model biofilm composed of four bacterial species belonging to four different genera (Rhodocyclus sp., Pseudomonas fluorescens, Kocuria varians, and Bacillus cereus), derived from a biofilm isolated from an industrial milk pasteurization unit. We demonstrate that the growth dynamics and equilibrium composition of this biofilm are highly reproducible. Based on its equilibrium composition, we show that the establishment of this 4-species biofilm is highly robust against initial, transient perturbations but less so towards continuous perturbations. By comparing biofilms formed from different numbers and combinations of the constituent species and by fitting a growth model to the experimental data, we reveal a network of dynamic, positive, and negative interactions that determine the final composition of the biofilm. Furthermore, we reveal that the molecular determinant of one negative interaction is the thiocillin I synthesized by the B. cereus strain, and demonstrate its importance for species distribution and its impact on robustness by mutational analysis of the biofilm ecosystem.

Peer review status:Published

21 Oct 2021Submitted to MicrobiologyOpen
22 Oct 2021Submission Checks Completed
22 Oct 2021Assigned to Editor
28 Oct 2021Review(s) Completed, Editorial Evaluation Pending
28 Oct 2021Editorial Decision: Revise Minor
16 Nov 20211st Revision Received
16 Nov 2021Submission Checks Completed
16 Nov 2021Assigned to Editor
16 Nov 2021Review(s) Completed, Editorial Evaluation Pending
17 Nov 2021Editorial Decision: Accept
Nov 2021Published in MicrobiologyOpen volume 10 issue 6. 10.1002/mbo3.1254