Preliminary indication of the role of AHL-dependent quorum sensing systems in calcium carbonate precipitation in Gram-negative bacteria

Paola Cacchio; Marika Pellegrini; Beatrice Farda; Rihab Djebaili; Silvia Tabacchioni; Maddalena Del Gallo; Paola Cacchio; Marika Pellegrini; Beatrice Farda; Rihab Djebaili; Silvia Tabacchioni; Maddalena Del Gallo

doi:10.3934/microbiol.2023035

AIMS Microbiology

2023, Volume 9, Issue 4: 692-711. doi: 10.3934/microbiol.2023035

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Research article

Preliminary indication of the role of AHL-dependent quorum sensing systems in calcium carbonate precipitation in Gram-negative bacteria

1.
Department of Life, Health and Environmental Sciences, University of L'Aquila, Coppito, 67100 L'Aquila, Italy
2.
Division Biotechnologies and Agroindustry, ENEA (Italian National Agency for New Technologies, Energy and Sustainable Economic Development), C.R. Casaccia, 000123 Rome, Italy

Received: 07 June 2023 Revised: 25 August 2023 Accepted: 04 September 2023 Published: 26 September 2023

Numerous microbial species participate in precipitation of carbonates in various natural environments, including soils, geological formations, freshwater biofilms and oceans. Despite the geochemical interest of such a biomineralization process, its molecular mechanisms and adaptive aspects remain poorly known. Many Gram-negative bacteria use cell-to-cell communication systems relying on N-acylhomoserine lactone (AHLs) signal molecules to express certain phenotypic traits in a density-dependent manner, a phenomenon referred as to quorum-sensing (QS). In this work, bacterial isolates collected from cave and rhizosphere soil were analyzed to study the occurrence of the AHL-mediated QS in bacterial calcium carbonate (CaCO₃) precipitation. To test the production of AHLs signal molecules, we cross-streaked Gram-negative calcifying strains, selected among the environmental strains studied, with the AHL-negative mutant Chromobacterium subtsugae strain CV026. Only Burkholderia ambifaria LMG 11351 was able to restore violacein production in CV026 among the tested strains. The constructed AHL-negative mutant of B. ambifaria LMG 11351 could not precipitate CaCO₃ on B-4 agar. Scanning Electron Microscopy (SEM) analysis on CaCO₃ crystals obtained in vitro shows crystals of different morphologies, calcified biofilms and bacteria in close contact with the precipitated crystals. In the inner layers of the bioliths deposited by B. ambifaria LMG 11351, a stream-like organization of the Burkholderia imprints was not detected by SEM. Our data provide preliminary evidence that the activation of AHL-regulated genes may be a prerequisite for in vitro bacterial carbonatogenesis, in some cases, confirming the specific role of bacteria as CaCO₃ precipitating agents. We enhance the understanding of bacterial CaCO₃ biomineralization and its potential biotechnology implications for QS-based strategies to enhance or decrease CaCO₃ precipitation through specific bacterial processes. The AHL-negative mutant of B. ambifaria LMG 11351 (a well-known plant growth-promoting bacterium) could also be used to study plant-bacteria interactions. The adaptive role of bacterial CaCO₃ biomineralization was also discussed.
- bacterial CaCO₃ precipitation,
- biomineralization,
- calcifying-bacteria,
- Gram-negative bacteria,
- quorum sensing,
- AHL-negative mutant,
- Burkholderia ambifaria
Citation: Paola Cacchio, Marika Pellegrini, Beatrice Farda, Rihab Djebaili, Silvia Tabacchioni, Maddalena Del Gallo. Preliminary indication of the role of AHL-dependent quorum sensing systems in calcium carbonate precipitation in Gram-negative bacteria[J]. AIMS Microbiology, 2023, 9(4): 692-711. doi: 10.3934/microbiol.2023035

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Abstract

Numerous microbial species participate in precipitation of carbonates in various natural environments, including soils, geological formations, freshwater biofilms and oceans. Despite the geochemical interest of such a biomineralization process, its molecular mechanisms and adaptive aspects remain poorly known. Many Gram-negative bacteria use cell-to-cell communication systems relying on N-acylhomoserine lactone (AHLs) signal molecules to express certain phenotypic traits in a density-dependent manner, a phenomenon referred as to quorum-sensing (QS). In this work, bacterial isolates collected from cave and rhizosphere soil were analyzed to study the occurrence of the AHL-mediated QS in bacterial calcium carbonate (CaCO₃) precipitation. To test the production of AHLs signal molecules, we cross-streaked Gram-negative calcifying strains, selected among the environmental strains studied, with the AHL-negative mutant Chromobacterium subtsugae strain CV026. Only Burkholderia ambifaria LMG 11351 was able to restore violacein production in CV026 among the tested strains. The constructed AHL-negative mutant of B. ambifaria LMG 11351 could not precipitate CaCO₃ on B-4 agar. Scanning Electron Microscopy (SEM) analysis on CaCO₃ crystals obtained in vitro shows crystals of different morphologies, calcified biofilms and bacteria in close contact with the precipitated crystals. In the inner layers of the bioliths deposited by B. ambifaria LMG 11351, a stream-like organization of the Burkholderia imprints was not detected by SEM. Our data provide preliminary evidence that the activation of AHL-regulated genes may be a prerequisite for in vitro bacterial carbonatogenesis, in some cases, confirming the specific role of bacteria as CaCO₃ precipitating agents. We enhance the understanding of bacterial CaCO₃ biomineralization and its potential biotechnology implications for QS-based strategies to enhance or decrease CaCO₃ precipitation through specific bacterial processes. The AHL-negative mutant of B. ambifaria LMG 11351 (a well-known plant growth-promoting bacterium) could also be used to study plant-bacteria interactions. The adaptive role of bacterial CaCO₃ biomineralization was also discussed.

Acknowledgments

We thank M. Giammatteo and L. Arrizza for assistance with SEM, S. Massimi for his assistance during laboratory work. We also thank Vittorio Venturi from ICGEB for providing us with the mutant strain of C. subtsugae CV026.

Conflict of interest

The authors declare no conflict of interest.

Author contributions

PC, MDG, and ST provided the concept and designed the work. PC, ST, MP, RD, and BF were involved in the literature review and manuscript writing. PC, MDG, and ST revised the final version of the manuscript. All authors approved the final version of the manuscript.

Funding options

The authors did not receive support from any organization for the submitted work.

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