High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization

Isenberg, Ruth Y; Christensen, David G.; Visick, Karen L.; Mandel, Mark J.

doi:10.1128/mbio.01671-22

Cited by 18 publications

(31 citation statements)

References 62 publications

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“…Increasing studies showed that c-di-GMP is essential for host colonization including Azoarcus sp. CIB, E. amylovora and V. fischeri (Fernandez-Llamosas et al, 2021;Isenberg et al, 2022;Kharadi et al, 2022). Our data indicate that c-di-GMP affects bacterial colonization on apple fruits via the potential receptor YdaK (Figure 12), which is consistent with that previously reported in Azoarcus sp.…”

Section: Ydak Does Not Affect the Antagonistic Activity Of B Velezens...supporting

confidence: 91%

“…C-di-GMP is a nearly ubiquitous bacterial nucleotide messenger that regulates a variety of important processes, including biofilm, antibiotic production and host colonization (Xu et al, 2018;Chou et al, 2020;Fernandez-Llamosas et al, 2021;Isenberg et al, 2022;Kharadi et al, 2022). In response to external stimuli, c-di-GMP is synthesized from 2 GTP molecules by diguanylate cyclases (DGCs) characterized by GGDEF domain.…”

Section: Introductionmentioning

confidence: 99%

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Cyclic di-GMP regulates bacterial colonization and further biocontrol efficacy of Bacillus velezensis against apple ring rot disease via its potential receptor YdaK

et al. 2022

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Bacillus species are among the most investigated beneficial bacteria and widely used in agricultural systems as biological control agents. Its biocontrol efficacy is controlled by diverse regulators. Cyclic diguanylate (c-di-GMP) is a nearly universal second messenger in bacteria and modulates various important physiological processes, including motility, biofilm formation, antifungal antibiotic production and host colonization. However, the impact of c-di-GMP on biocontrol efficacy of beneficial bacteria is unknown. Bacillus velezensis PG12 is an effective biocontrol strain against apple ring rot disease caused by Botryosphaeria dothidea. In this study, the contribution of c-di-GMP to biocontrol efficacy of B. velezensis PG12 was investigated. Deletion of single gene encoding diguanylate cyclase or phosphodiesterase did not affect its biocontrol efficacy against apple ring rot. However, artificial modulation of c-di-GMP level in the cells leads to a significant change of biocontrol efficacy, suggesting that c-di-GMP positively regulates biocontrol efficacy of B. velezensis PG12 against apple ring rot disease. More evidences indicate that c-di-GMP does not affect the antagonistic activity of B. velezensis PG12 against B. dothidea in vitro and in vivo, but positively regulates biofilm formation of B. velezensis PG12 and its colonization on apple fruits. Importantly, deletion of ydaK could rescue the inhibition of biofilm formation, bacterial colonization and biocontrol efficacy caused by low c-di-GMP level, indicating that YdaK is the potential c-di-GMP receptor to regulate biofilm formation, colonization and effective biological control. However, YdaK did not affect the antagonistic activity of B. velezensis PG12 against B. dothidea. Based on these findings, we propose that c-di-GMP regulates biofilm formation, subsequently the bacterial colonization on apple fruits and thus biocontrol efficacy of B. velezensis through its receptor YdaK. This is the first report showing that c-di-GMP plays a role in biocontrol efficacy of beneficial bacteria.

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Section: Ydak Does Not Affect the Antagonistic Activity Of B Velezens...supporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Cyclic di-GMP regulates bacterial colonization and further biocontrol efficacy of Bacillus velezensis against apple ring rot disease via its potential receptor YdaK

et al. 2022

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“…However, it is not unreasonable to imagine that although cellulose can have a positive role during the early steps of this plant–bacteria interaction, a continuous overproduction of this β-glucan over the whole infection process, e.g., through the infection thread, could have a pernicious effect for the symbiotic establishment. This seems also to be the case in other bacteria-host associations, where the overproduction of cellulose generated by high c-di-GMP intracellular levels negatively affects the production of other EPS involved in the symbiotic process [ 52 ].…”

Section: Discussionmentioning

confidence: 99%

The Role of Two Linear β-Glucans Activated by c-di-GMP in Rhizobium etli CFN42

Pérez-Mendoza

Romero-Jiménez

Carvajal

et al. 2022

Biology

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Bacterial exopolysaccharides (EPS) have been implicated in a variety of functions that assist in bacterial survival, colonization, and host–microbe interactions. Among them, bacterial linear β-glucans are polysaccharides formed by D-glucose units linked by β-glycosidic bonds, which include curdlan, cellulose, and the new described Mixed Linkage β-Glucan (MLG). Bis-(3′,5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a universal bacterial second messenger that usually promote EPS production. Here, we report Rhizobium etli as the first bacterium capable of producing cellulose and MLG. Significant amounts of these two β-glucans are not produced under free-living laboratory conditions, but their production is triggered upon elevation of intracellular c-di-GMP levels, both contributing to Congo red (CR+) and Calcofluor (CF+) phenotypes. Cellulose turned out to be more relevant for free-living phenotypes promoting flocculation and biofilm formation under high c-di-GMP conditions. None of these two EPS are essential for attachment to roots of Phaseolus vulgaris, neither for nodulation nor for symbiotic nitrogen fixation. However, both β-glucans separately contribute to the fitness of interaction between R. etli and its host. Overproduction of these β-glucans, particularly cellulose, appears detrimental for symbiosis. This indicates that their activation by c-di-GMP must be strictly regulated in time and space and should be controlled by different, yet unknown, regulatory pathways.

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“…Based on these results, we hypothesize that increased cyclic-di-GMP in the prophage KO strains leads to reduced motility and increased biofilm formation. Increased cyclic-di-GMP levels have also been reported to reduce motility and impact biofilm morphology in Vibrio fischeri [80]. It has also been reported that the influence of a Vibrio anguillarum prophage is repressed by specific quorum sensing mechanisms and that this action results in an increase in biofilm formation [81].…”

Section: Discussionmentioning

confidence: 99%

Prophages regulateShewanella fidelis3313 motility and biofilm formation: implications for gut colonization dynamics inCiona robusta

Natarajan

Gibboney

Young

et al. 2022

Preprint

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Prophages are viruses that integrate into the genomes of bacteria, which then become lysogens. Lysogens are abundant in the gut of animals, where prophages are known to influence their metabolic pathways and other traits. However, the potential influence of prophages on the gut microbiota-host immune axis in animals remains poorly understood. Here, we investigated the influence of prophages in a marine lysogen,Shewanella fidelis3313, a prevalent member of the gut microbiome of the model tunicate,Ciona robusta. Two prophages, SfPat and SfMu1, were deleted individually and in combination using homologous recombination to observe the effects of these prophages on processes involved in gut colonization. We report here that in vitro, these prophages enhance motility and negatively impact biofilm formation ofS. fidelis 3313. To understand the in vivo impact of these prophage-induced changes in bacterial traits, we exposed metamorphic stage 4Cionajuveniles (the stage that correlates to first feeding and subsequent gut colonization) to both wildtype (WT) and modified strains ofS. fidelis 3313. When colonizing theCionagut, the WT strain experiences an upregulation ofpdeB, a phosphodiesterase known to degrade cyclic di-GMP, a dinucleotide messenger that can positively influence biofilm formation while negatively regulating motility. WT colonization and upregulation ofpdeBalso correlates to a downregulation of theCionagut immune effector, VCBP-C. This study reveals an influence of prophages on bacterial traits and host immune response in the gut of a model organism. Our findings highlight the importance of interkingdom signaling between prophages, bacteria, and their animal hosts in regulating the gut microbiota-host immune axis.

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High Levels of Cyclic Diguanylate Interfere with Beneficial Bacterial Colonization

Cited by 18 publications

References 62 publications

Cyclic di-GMP regulates bacterial colonization and further biocontrol efficacy of Bacillus velezensis against apple ring rot disease via its potential receptor YdaK

Cyclic di-GMP regulates bacterial colonization and further biocontrol efficacy of Bacillus velezensis against apple ring rot disease via its potential receptor YdaK

The Role of Two Linear β-Glucans Activated by c-di-GMP in Rhizobium etli CFN42

Prophages regulateShewanella fidelis3313 motility and biofilm formation: implications for gut colonization dynamics inCiona robusta

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