Abstract

Background:Recent reports exploring the role of gradients of quorum sensing (QS) signals in functional activated sludge have raised the question of whether shared systems of signalling synthesis and degradation, or quorum quenching (QQ), across the community inform of the means by which QS biology regulate floccular and granular biofilm assembly.Aims:In this study, we aimed to explore the species origin and interactive role of QS and QQ activities in such highly diverse microbial biofilm communities.Methods:Here, such aims were addressed systematically by a comprehensive multi-pronged RNA-sequencing, microbiological and analytical chemistry experimental approach, using two related but independently evolved floccular and granular sludge communities.Results:Our data revealed a distinct difference between the QS and QQ potentials of the two communities, with different species largely displaying either QS or QQ functions. The floccular sludge community showed a high rate of QQ activity, and this rate was dependent on the acyl chain length demonstrating specificity of degradation. When the floccular biomass was transformed into the granular sludge, the QQ activity of the community was reduced by 30%. N-acyl homoserine lactones with four to eight carbons on the acyl chain accumulated at the granular stage, and their concentrations were at least threefold higher than those of the floccular stage. These findings corroborated meta-community analysis where a major shift in the dominant species from potential signal quenchers to producers was observed during the transition from flocs to granules, indicating the role of species composition and associated signalling activities in coordinating community behaviours.Conclusions:This study suggests that QQ has an important function in regulating community level QS signalling, and provides a mechanistic insight into the role of QS biology in complex community assembly.

Highlights

  • In most natural and engineered ecosystems, bacteria predominantly reside in structured communities, in aggregations commonly known as microbial biofilms.[1]

  • To determine whether acyl homoserine lactone (AHL)-specific quorum quenching (QQ) activity was present in this model system, synthetic AHLs were added individually or as a mixture to the floccular sludge to characterise the rates of signal degradation

  • Communication via diffusible signalling molecules has been proposed to be one of the important interactions among species of diverse origins,[3] and there is growing evidence that complex communities in natural environments produce quorum sensing (QS) signals in situ to regulate different community behaviours.[14,16,18,19]. These findings have demonstrated the roles of QS in complex communities, the question of how competing activities, such as the QQ modulation of QS in complex communities, are mediated remains to be addressed

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Summary

Introduction

In most natural and engineered ecosystems, bacteria predominantly reside in structured communities, in aggregations commonly known as microbial biofilms.[1] These microbial consortia can be comprised of hundreds to thousands of bacterial species with varying metabolic capabilities and collectively displaying community level properties that are distinct from the planktonic cells.[2,3] The overall composition and function of complex biofilms is typically driven by interactions between the different microbial species.[1,3] Understanding the dynamics of interspecies interactions within such complex multi-species biofilms is challenging, yet important in order to control and regulate key ecosystem functions These include, e.g., the engineering of highly stable and sustainable microbial communities for water and wastewater treatment, or the treatment of biofilm-related diseases. CONCLUSIONS: This study suggests that QQ has an important function in regulating community level QS signalling, and provides a mechanistic insight into the role of QS biology in complex community assembly

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