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Biofilm formation assessment in Sinorhizobium meliloti reveals interlinked control with surface motility

BACKGROUND: Swarming motility and biofilm formation are opposite, but related surface-associated behaviors that allow various pathogenic bacteria to colonize and invade their hosts. In Sinorhizobium meliloti, the alfalfa endosymbiont, these bacterial processes and their relevance for host plant colo...

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Autores principales: Amaya-Gómez, Carol V, Hirsch, Ann M, Soto, María J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4381460/
https://www.ncbi.nlm.nih.gov/pubmed/25887945
http://dx.doi.org/10.1186/s12866-015-0390-z
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author Amaya-Gómez, Carol V
Hirsch, Ann M
Soto, María J
author_facet Amaya-Gómez, Carol V
Hirsch, Ann M
Soto, María J
author_sort Amaya-Gómez, Carol V
collection PubMed
description BACKGROUND: Swarming motility and biofilm formation are opposite, but related surface-associated behaviors that allow various pathogenic bacteria to colonize and invade their hosts. In Sinorhizobium meliloti, the alfalfa endosymbiont, these bacterial processes and their relevance for host plant colonization are largely unexplored. Our previous work demonstrated distinct swarming abilities in two S. meliloti strains (Rm1021 and GR4) and revealed that both environmental cues (iron concentration) and bacterial genes (fadD, rhb, rirA) play crucial roles in the control of surface motility in this rhizobial species. In the current study, we investigate whether these factors have an impact on the ability of S. meliloti to establish biofilms and to colonize host roots. RESULTS: We found that strain GR4, which is less prone to translocate on solid surfaces than strain Rm1021, is more efficient in developing biofilms on glass and plant root surfaces. High iron conditions, known to prevent surface motility in a wild-type strain of S. meliloti, promote biofilm development in Rm1021 and GR4 strains by inducing the formation of more structured and thicker biofilms than those formed under low iron levels. Moreover, three different S. meliloti mutants (fadD, rhb, and rirA) that exhibit an altered surface translocation behavior compared with the wild-type strain, establish reduced biofilms on both glass and alfalfa root surfaces. Iron-rich conditions neither rescue the defect in biofilm formation shown by the rhb mutant, which is unable to produce the siderophore rhizobactin 1021 (Rhb1021), nor have any impact on biofilms formed by the iron-response regulator rirA mutant. On the other hand, S. meliloti FadD loss-of-function mutants do not establish normal biofilms irrespective of iron levels. CONCLUSIONS: Our studies show that siderophore Rhb1021 is not only required for surface translocation, but also for biofilm formation on glass and root surfaces by strain Rm1021. In addition, we present evidence for the existence of control mechanisms that inversely regulate swarming and biofilm formation in S. meliloti, and that contribute to efficient plant root colonization. One of these mechanisms involves iron levels and the iron global regulator RirA. The other mechanism involves the participation of the fatty acid metabolism-related enzyme FadD. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-015-0390-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-43814602015-04-02 Biofilm formation assessment in Sinorhizobium meliloti reveals interlinked control with surface motility Amaya-Gómez, Carol V Hirsch, Ann M Soto, María J BMC Microbiol Research Article BACKGROUND: Swarming motility and biofilm formation are opposite, but related surface-associated behaviors that allow various pathogenic bacteria to colonize and invade their hosts. In Sinorhizobium meliloti, the alfalfa endosymbiont, these bacterial processes and their relevance for host plant colonization are largely unexplored. Our previous work demonstrated distinct swarming abilities in two S. meliloti strains (Rm1021 and GR4) and revealed that both environmental cues (iron concentration) and bacterial genes (fadD, rhb, rirA) play crucial roles in the control of surface motility in this rhizobial species. In the current study, we investigate whether these factors have an impact on the ability of S. meliloti to establish biofilms and to colonize host roots. RESULTS: We found that strain GR4, which is less prone to translocate on solid surfaces than strain Rm1021, is more efficient in developing biofilms on glass and plant root surfaces. High iron conditions, known to prevent surface motility in a wild-type strain of S. meliloti, promote biofilm development in Rm1021 and GR4 strains by inducing the formation of more structured and thicker biofilms than those formed under low iron levels. Moreover, three different S. meliloti mutants (fadD, rhb, and rirA) that exhibit an altered surface translocation behavior compared with the wild-type strain, establish reduced biofilms on both glass and alfalfa root surfaces. Iron-rich conditions neither rescue the defect in biofilm formation shown by the rhb mutant, which is unable to produce the siderophore rhizobactin 1021 (Rhb1021), nor have any impact on biofilms formed by the iron-response regulator rirA mutant. On the other hand, S. meliloti FadD loss-of-function mutants do not establish normal biofilms irrespective of iron levels. CONCLUSIONS: Our studies show that siderophore Rhb1021 is not only required for surface translocation, but also for biofilm formation on glass and root surfaces by strain Rm1021. In addition, we present evidence for the existence of control mechanisms that inversely regulate swarming and biofilm formation in S. meliloti, and that contribute to efficient plant root colonization. One of these mechanisms involves iron levels and the iron global regulator RirA. The other mechanism involves the participation of the fatty acid metabolism-related enzyme FadD. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-015-0390-z) contains supplementary material, which is available to authorized users. BioMed Central 2015-03-03 /pmc/articles/PMC4381460/ /pubmed/25887945 http://dx.doi.org/10.1186/s12866-015-0390-z Text en © Amaya-Gómez et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Amaya-Gómez, Carol V
Hirsch, Ann M
Soto, María J
Biofilm formation assessment in Sinorhizobium meliloti reveals interlinked control with surface motility
title Biofilm formation assessment in Sinorhizobium meliloti reveals interlinked control with surface motility
title_full Biofilm formation assessment in Sinorhizobium meliloti reveals interlinked control with surface motility
title_fullStr Biofilm formation assessment in Sinorhizobium meliloti reveals interlinked control with surface motility
title_full_unstemmed Biofilm formation assessment in Sinorhizobium meliloti reveals interlinked control with surface motility
title_short Biofilm formation assessment in Sinorhizobium meliloti reveals interlinked control with surface motility
title_sort biofilm formation assessment in sinorhizobium meliloti reveals interlinked control with surface motility
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4381460/
https://www.ncbi.nlm.nih.gov/pubmed/25887945
http://dx.doi.org/10.1186/s12866-015-0390-z
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