Motile bacteria leverage bioconvection for eco-physiological benefits in a natural aquatic environment

Francesco Di Nezio; Samuele Roman; Antoine Buetti-Dinh; Oscar Sepúlveda Steiner; Damien Bouffard; Anupam Sengupta; Nicola Storelli

doi:10.3389/fmicb.2023.1253009

Motile bacteria leverage bioconvection for eco-physiological benefits in a natural aquatic environment

Front Microbiol. 2023 Dec 13:14:1253009. doi: 10.3389/fmicb.2023.1253009. eCollection 2023.

Authors

Francesco Di Nezio^{1

2}, Samuele Roman^{1

3}, Antoine Buetti-Dinh¹, Oscar Sepúlveda Steiner^{4

5}, Damien Bouffard^{4

6}, Anupam Sengupta⁷, Nicola Storelli^{1

2}

Affiliations

¹ Department of Environment, Constructions, and Design, Institute of Microbiology, University of Applied Sciences and Arts of Southern Switzerland (SUPSI), Mendrisio, Switzerland.
² Department of Plant Sciences, University of Geneva, Geneva, Switzerland.
³ Alpine Biology Center Foundation, Bellinzona, Switzerland.
⁴ Department of Surface Waters - Research and Management, Swiss Federal Institute of Aquatic Science and Technology (Eawag), Kastanienbaum, Switzerland.
⁵ Civil and Environmental Engineering, University of California, Davis, Davis, CA, United States.
⁶ Faculty of Geosciences and Environment, Institute of Earth Surface Dynamics, University of Lausanne, Lausanne, Switzerland.
⁷ Department of Physics and Materials Science, Physics of Living Matter Group, Luxembourg City, Luxembourg.

Abstract

Introduction: Bioconvection, a phenomenon characterized by the collective upward swimming of motile microorganisms, has mainly been investigated within controlled laboratory settings, leaving a knowledge gap regarding its ecological implications in natural aquatic environments. This study aims to address this question by investigating the influence of bioconvection on the eco-physiology of the anoxygenic phototrophic sulfur bacteria community of meromictic Lake Cadagno.

Methods: Here we comprehensively explore its effects by comparing the physicochemical profiles of the water column and the physiological traits of the main populations of the bacterial layer (BL). The search for eco-physiological effects of bioconvection involved a comparative analysis between two time points during the warm season, one featuring bioconvection (July) and the other without it (September).

Results: A prominent distinction in the physicochemical profiles of the water column centers on light availability, which is significantly higher in July. This minimum threshold of light intensity is essential for sustaining the physiological CO₂ fixation activity of Chromatium okenii, the microorganism responsible for bioconvection. Furthermore, the turbulence generated by bioconvection redistributes sulfides to the upper region of the BL and displaces other microorganisms from their optimal ecological niches.

Conclusion: The findings underscore the influence of bioconvection on the physiology of C. okenii and demonstrate its functional role in improving its metabolic advantage over coexisting phototrophic sulfur bacteria. However, additional research is necessary to confirm these results and to unravel the multiscale processes activated by C. okenii's motility mechanisms.

Keywords: Lake Cadagno; bioconvection; eco-physiology; meromixis; sulfur bacteria.

Grants and funding

Funding was provided 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). The quality of the scientific equipment used during monitoring was made possible by cantonal funding for the mandate “Indagini, perizie e consulenza in Microbiologia ambientale” of the Department of “socialità e sanità” (DSS). AS thanks the ATTRACT Investigator Grant (No. A17/MS/11572821/MBRACE) and FNR-CORE Grant (No. C19/MS/13719464/TOPOFLUME/Sengupta) from the Luxembourg National Research Fund for supporting this work.