An intriguing relationship between the cyclic diguanylate signaling system and horizontal gene transfer

Madsen, Jonas Stenløkke; Hylling, Ole; Jacquiod, Samuel; Pécastaings, Sophia; Hansen, Lars; Riber, Leise; Vestergaard, Gisle; Sørensen, Søren J.

doi:10.1038/s41396-018-0183-0

Cited by 22 publications

(23 citation statements)

References 19 publications

(24 reference statements)

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“…Interestingly, pQBR55 carries an RsmA homologue (PQBR55_0192), which might directly affect GacA/S or cyclic-di-GMP signalling to cause small colonies in P. fluorescens [35].…”

Section: Resultsmentioning

confidence: 99%

Extremely fast amelioration of plasmid fitness costs by multiple functionally diverse pathways

et al. 2020

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The acquisition of plasmids is often accompanied by fitness costs such that compensatory evolution is required to allow plasmid survival, but it is unclear whether compensatory evolution can be extensive or rapid enough to maintain plasmids when they are very costly. The mercury-resistance plasmid pQBR55 drastically reduced the growth of its host, Pseudomonas fluorescens SBW25, immediately after acquisition, causing a small colony phenotype. However, within 48 h of growth on agar plates we observed restoration of the ancestral large colony morphology, suggesting that compensatory mutations had occurred. Relative fitness of these evolved strains, in lab media and in soil microcosms, varied between replicates, indicating different mutational mechanisms. Using genome sequencing we identified that restoration was associated with chromosomal mutations in either a hypothetical DNA-binding protein PFLU4242, RNA polymerase or the GacA/S two-component system. Targeted deletions in PFLU4242, gacA or gacS recapitulated the ameliorated phenotype upon plasmid acquisition, indicating three distinct mutational pathways to compensation. Our data shows that plasmid compensatory evolution is fast enough to allow survival of a plasmid despite it imposing very high fitness costs upon its host, and indeed may regularly occur during the process of isolating and selecting individual plasmid-containing clones.

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“…Interestingly, pQBR55 carries an RsmA homologue (PQBR55_0192), which might directly affect GacA/S or cyclic-di-GMP signalling to cause small colonies in P. fluorescens [35].…”

Section: Resultsmentioning

confidence: 99%

Extremely fast amelioration of plasmid fitness costs by multiple functionally diverse pathways

et al. 2020

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“…Genes associated with cell signaling were also detected in viromes from the surface and oxycline waters of the ETSP ODWC [ 22 ], and in cultivated viral isolates [ 78 ]. Selective pressure may exist to retain DGC genes in viral elements since they can enhance rates of conjugative plasmid transfer in anaerobic bacterial strains via the production of the secondary messenger cyclic diguanylate (c-di-GMP) [ 79 ]. This could enhance host fitness in ODWCs by increasing gene transfer.…”

Section: Resultsmentioning

confidence: 99%

Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline

et al. 2020

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Little is known about viruses in oxygen-deficient water columns (ODWCs). In surface ocean waters, viruses are known to act as gene vectors among susceptible hosts. Some of these genes may have metabolic functions and are thus termed auxiliary metabolic genes (AMGs). AMGs introduced to new hosts by viruses can enhance viral replication and/or potentially affect biogeochemical cycles by modulating key microbial pathways. Here we identify 748 viral populations that cluster into 94 genera along a vertical geochemical gradient in the Cariaco Basin, a permanently stratified and euxinic ocean basin. The viral communities in this ODWC appear to be relatively novel as 80 of these viral genera contained no reference viral sequences, likely due to the isolation and unique features of this system. We identify viral elements that encode AMGs implicated in distinctive processes, such as sulfur cycling, acetate fermentation, signal transduction, [Fe–S] formation, and N-glycosylation. These AMG-encoding viruses include two putative Mu-like viruses, and viral-like regions that may constitute degraded prophages that have been modified by transposable elements. Our results provide an insight into the ecological and biogeochemical impact of viruses oxygen-depleted and euxinic habitats.

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“…harbor different types of MGEs including prophages ( Tapia et al, 2012 ; Covarrubias et al, 2018 ), plasmids (reviewed in Quatrini et al, 2016 ) and integrative conjugative elements (ICEs) ( Bustamante et al, 2012 ; Acuña et al, 2013 ). Albeit a few reports on the occurrence of c-di-GMP pathway modules on MGEs exist ( Bordeleau et al, 2010 ; Madsen et al, 2018 ), bioinformatic analyses of several Acidithiobacillus genomes point out the frequent occurrence of c-di-GMP related elements in this taxon’s mobilome.…”

Section: Resultsmentioning

confidence: 99%

Nucleotide Second Messenger-Based Signaling in Extreme Acidophiles of the Acidithiobacillus Species Complex: Partition Between the Core and Variable Gene Complements

et al. 2019

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Cyclic and linear nucleotides are key elements of the signal transduction networks linking perception of the environment to specific cellular behavior of prokaryotes. These molecular mechanisms are particularly important in bacteria exposed to different, and frequently simultaneous, types of extreme conditions. This is the case in acidithiobacilli, a group of extremophilic bacteria thriving in highly acidic biotopes, that must also cope with significant variations in temperature, osmotic potentials and concentrations of various transition metals and metalloids. Environmental cues sensed by bacteria are transduced into differential levels of nucleotides acting as intracellular second messengers, promoting the activation or inhibition of target components and eliciting different output phenotypes. Cyclic (c) di-GMP, one of the most common bacterial second messengers, plays a key role in lifestyle changes in many bacteria, including acidithiobacilli. The presence of functional c-di-GMP-dependent signal transduction pathways in representative strains of the best-known linages of this species complex has been reported. However, a comprehensive panorama of the c-di-GMP modulated networks, the cognate input signals and output responses, are still missing for this group of extremophiles. Moreover, little fundamental understanding has been gathered for other nucleotides acting as second messengers. Taking advantage of the increasing number of sequenced genomes of the taxon, here we address the challenge of disentangling the nucleotide-driven signal transduction pathways in this group of polyextremophiles using comparative genomic tools and strategies. Results indicate that the acidithiobacilli possess all the genetic elements required to establish functional transduction pathways based in three different nucleotide-second messengers: (p)ppGpp, cyclic AMP (cAMP), and c-di-GMP. The elements related with the metabolism and transduction of (p)ppGpp and cAMP appear highly conserved, integrating signals related with nutrient starvation and polyphosphate metabolism, respectively. In contrast, c-di-GMP networks appear diverse and complex, differing both at the species and strain levels. Molecular elements of c-di-GMP metabolism and transduction were mostly found scattered along the flexible genome of the acidithiobacilli, allowing the identification of probable control modules that could be critical for substrate colonization, biofilm development and intercellular interactions. These may ultimately convey increased endurance to environmental stress and increased potential for gene sharing and adaptation to changing conditions.

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An intriguing relationship between the cyclic diguanylate signaling system and horizontal gene transfer

Cited by 22 publications

References 19 publications

Extremely fast amelioration of plasmid fitness costs by multiple functionally diverse pathways

Extremely fast amelioration of plasmid fitness costs by multiple functionally diverse pathways

Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline

Nucleotide Second Messenger-Based Signaling in Extreme Acidophiles of the Acidithiobacillus Species Complex: Partition Between the Core and Variable Gene Complements

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