Viewing biofilm formation through a multifocal lens of physics and biology
Binu Kundukad A # , James C. S. Ho A B # , Sudarsan Mugunthan A , Lan Li Wong A , Scott A. Rice C , Atul N. Parikh A B D , Thomas Seviour A E , Jamie Hinks H and Staffan Kjelleberg A F G *A Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore.
B Institute for Digital Molecular Analytics and Science, Nanyang Technological University, Singapore.
C CSIRO, Agriculture and Food, Microbiomes for One Systems Health, Canberra, ACT, Australia.
D Department of Biomedical Engineering, University of California, Davis, CA, USA.
E WATEC Aarhus University Centre for Water Technology, Aarhus, Denmark.
F School of Biological Sciences, Nanyang Technological University, Singapore.
G School of Biological, Earth and Environmental Sciences, University of New South Wales, NSW, Australia.
H Deceased. Formerly at Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore.
Binu Kundukad is a senior research fellow at the Singapore Centre for Environmental Life Sciences Engineering (SCELSE), Nanyang Technological University, Singapore. With a background in physics, her research interest is in developing and using biophysical tools and methods to understand biological problems. She is particularly interested in understanding how the mechanical properties of biofilm matrix, such as viscosity and elasticity, influence bacterial behaviour and biofilm formation. |
James C. S. Ho is a senior research fellow at SCELSE. His research focuses on the assembly of functional, multi-length scale biomolecular complexes and using them to understand complex biological and biophysical processes. |
Sudarsan Mugunthan is a graduate student at SCELSE. His research focuses on the role of extracellular DNA/RNA in Pseudomonas biofilms and the regulation of eDNA and eRNA secretion. |
Lan Li Wong is a graduate student at SCELSE. She works on structure–function characterisation of extracellular polymeric substances forming anammox granule biofilms, with a focus on surface layer proteins. |
Scott A. Rice is the director of Microbiomes for One Systems Health at CSIRO, Australia. His research focuses on microbial cell–cell interactions and mechanisms of adaptation to environmental conditions. The goal has been to develop a deep understanding of the mechanisms by which bacteria mediate these responses and the impacts of those responses on the behaviour and function of bacteria. |
Atul N. Parikh is a professor at the University of California, Davis. He is also serving as a Visiting Professor at SCELSE. His current research includes fundamental studies of dynamic self-assembly, active interfaces, and physical compartmentalisation in soft and living material systems. |
Thomas Seviour is an associate professor at the Aarhus University, Denmark. His research aims to elucidate structure–function relationships of microbial biointerfaces in biofilms and bioprocesses of industrial and environmental significance. This understanding will lead to more precise biofilm and bioprocess control strategies, and may inform new approaches towards resource recovery. |
Jamie Hinks was a senior principal research fellow at SCELSE. Jamie was an environmental microbiologist. He was interested in how small molecules, either native or exogenous, interact with the microbial envelope and the reactions these mediate. |
Staffan Kjelleberg is an adviser to SCELSE and Distinguished University Professor at NTU. He has made major contributions to microbial ecology. His studies on bacterial adaptive responses and biofilm biology have received strong international recognition and have illuminated biofilm as the predominant mode of bacterial life in the environment. |
Microbiology Australia 44(2) 69-74 https://doi.org/10.1071/MA23021
Submitted: 22 March 2023 Accepted: 9 May 2023 Published: 24 May 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the ASM. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Recent studies on the formation, organisation and dynamics of biofilms highlight the interplay between physical forces and biological programs. Two complementary generalised pathways that explain the mechanisms driving biofilm formation have emerged. In the first pathway, where physical forces precede the biological program, the initial expansion of cells leads to cell clustering or aggregation prior to the production of extracellular polymeric substances (EPS). The second pathway describes an initial biologically prompted production of EPS, which introduces new biophysical interactions within the EPS, such as by phase separation, macromolecular crowding, excluded volume interactions and intermolecular cross-linking. In practice, which of the two pathways is adopted is ultimately determined by the specificities of the biofilm and the local microenvironment, each leading to the formation of robust, viscoelastic biofilm. Within this framework, we further highlight here recent findings on the role of higher-order structures in matrix gelation and phase separation of EPS in promoting the clustering of bacteria. We assert that examining biofilms through the combined lens of physics and biology promises new and significant methodological and conceptual advancements in our understanding of biofilms.
Keywords: biofilms, EPS, extracellular polymeric substances, matrix, phase separation, viscoelasticity.
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