[en] Isolating microorganisms from natural environments for cultivation under optimized laboratory settings has markedly improved our understanding of microbial ecology. Artificial growth conditions often diverge from those in natural ecosystems, forcing wild isolates into distinct selective pressures, resulting in diverse eco-physiological adaptations mediated by modification of key phenotypic traits. For motile microorganisms we still lack a biophysical understanding of the relevant traits emerging during domestication and their mechanistic interplay driving short-to-long-term microbial adaptation under laboratory conditions. Using microfluidics, atomic force microscopy, quantitative imaging, and mathematical modeling, we study phenotypic adaptation of Chromatium okenii, a motile phototrophic purple sulfur bacterium from meromictic Lake Cadagno, grown under laboratory conditions over multiple generations. Our results indicate that naturally planktonic C. okenii leverage shifts in cell-surface adhesive interactions, synergistically with changes in cell morphology, mass density, and distribution of intracellular sulfur globules, to suppress their swimming traits, ultimately switching to a sessile lifeform. A computational model of cell mechanics confirms the role of such phenotypic shifts in suppressing the planktonic lifeform. By investigating key phenotypic traits across different physiological stages of lab-grown C. okenii, we uncover a progressive loss of motility during the early stages of domestication, followed by concomitant deflagellation and enhanced surface attachment, ultimately driving the transition of motile sulfur bacteria to a sessile state. Our results establish a mechanistic link between suppression of motility and surface attachment via phenotypic changes, underscoring the emergence of adaptive fitness under laboratory conditions at the expense of traits tailored for natural environments.
Disciplines :
Physique, chimie, mathématiques & sciences de la terre: Multidisciplinaire, généralités & autres
Auteur, co-auteur :
Di Nezio, Francesco; Department of Environment, Institute of Microbiology, Constructions and Design, University of Applied Sciences and Arts of Southern Switzerland (SUPSI), Mendrisio, Switzerland ; Microbiology Unit, Department of Plant Sciences, University of Geneva, Geneva, Switzerland
ONG, Irvine ; University of Luxembourg > Faculty of Science, Technology and Medicine > Department of Physics and Materials Science > Team Anupam SENGUPTA
Riedel, René; Physics of Living Matter Group, Department of Physics and Materials Science, University of Luxembourg, Luxembourg City, Luxembourg
Goshal, Arkajyoti; Physics of Living Matter Group, Department of Physics and Materials Science, University of Luxembourg, Luxembourg City, Luxembourg
DHAR, Jayabrata ; University of Luxembourg > Faculty of Science, Technology and Medicine > Department of Physics and Materials Science > Team Anupam SENGUPTA ; Department of Mechanical Engineering, National Institute of Technology, Durgapur, India
Roman, Samuele; Department of Environment, Institute of Microbiology, Constructions and Design, University of Applied Sciences and Arts of Southern Switzerland (SUPSI), Mendrisio, Switzerland ; Alpine Biology Center Foundation, Bellinzona, Switzerland
Storelli, Nicola; Department of Environment, Institute of Microbiology, Constructions and Design, University of Applied Sciences and Arts of Southern Switzerland (SUPSI), Mendrisio, Switzerland ; Microbiology Unit, Department of Plant Sciences, University of Geneva, Geneva, Switzerland
Synergistic phenotypic adaptations of motile purple sulphur bacteria Chromatium okenii during lake-to-laboratory domestication.
Date de publication/diffusion :
22 octobre 2024
Titre du périodique :
PLoS ONE
eISSN :
1932-6203
Maison d'édition :
Public Library of Science (PLoS), Etats-Unis
Volume/Tome :
19
Fascicule/Saison :
10
Pagination :
e0310265
Peer reviewed :
Peer reviewed vérifié par ORBi
Focus Area :
Physics and Materials Science
Objectif de développement durable (ODD) :
6. Eau propre et assainissement 11. Villes et communautés durables 14. Vie aquatique 13. Mesures relatives à la lutte contre les changements climatiques
H2020 - 897629 - BIOMIMIC - BIOphysics of MIcrobe-Microplastic Interactions and Colonization
Projet FnR :
FNR11572821 - Biophysics Of Microbial Adaptation To Fluctuations In The Environment, 2017 (15/05/2018-14/05/2023) - Anupam Sengupta FNR13719464 - Topological Fluid Mechanics: Decoding Emergent Dynamics In Anisotropic Fluids And Living Systems, 2019 (01/09/2020-31/08/2023) - Anupam Sengupta FNR13563560 - Microbial Signal Transduction Under Fluctuating Fields, 2019 (01/07/2019-30/06/2023) - Arkajyoti Ghoshal
Intitulé du projet de recherche :
R-AGR-3401 - A17/MS/11572821/MBRACE - part UL - SENGUPTA Anupam R-AGR-3692 - C19/MS/13719464/TOPOFLUME - SENGUPTA Anupam
Organisme subsidiant :
Fonds National de la Recherche Luxembourg Fonds National de la Recherche Luxembourg Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung H2020 Marie Skłodowska-Curie Actions Fonds National de la Recherche Luxembourg Institute of Microbiology SUPSI Union Européenne
Subventionnement (détails) :
This work was supported by the Swiss National Science Foundation (grant number 315230–179264) and by the Institute of Microbiology (IM) of the University of Applied Sciences and Arts of Southern Switzerland (SUPSI) through the financing from the Department of “Socialità e Sanità” (DSS) of the Canton Ticino. I.L.H.O. thanks the support from Marie Skłodowska-Curie Actions Individual Fellowship (BIOMIMIC grant agreement number 897629). Support of the Luxembourg National Research Fund’s AFR-Grant (Grant no. 13563560), the ATTRACT Investigator Grant, A17/MS/11572821/MBRACE (to A.S.), and the FNR-CORE Grant (No. C19/MS/13719464/TOPOFLUME/Sengupta) are gratefully acknowledged.
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