You are what you talk: quorum sensing induces individual morphologies and cell division modes in <i>Dinoroseobacter shibae</i>

Patzelt, Diana; Wang, Hui; Buchholz, Ina; Rohde, Manfred; Gröbe, Lothar; Pradella, Silke; Neumann, Alexander; Schulz, Stefan; Heyber, Steffi; Münch, Karin; Münch, Richard; Jahn, Dieter; Wagner‐Döbler, Irene; Tomasch, Jürgen

doi:10.1038/ismej.2013.107

Cited by 67 publications

(124 citation statements)

References 66 publications

(63 reference statements)

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“…Further, the authors of this study convincingly demonstrated that the phenotype of a luxI1 mutant could be restored by the addition of the corresponding C 18 -HSL at saturating concentrations. Additional transcriptome analyses in the background of this deletion mutant further supported the hypothesis of the AIdependent morphological cell variability (25).…”

Section: Bacterial Qs: a System Thought To Coordinate Cells Instead Osupporting

confidence: 58%

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Phenotypic Heterogeneity, a Phenomenon That May Explain Why Quorum Sensing Does Not Always Result in Truly Homogenous Cell Behavior

Grote

Krysciak

Streit

2015

Appl Environ Microbiol

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Phenotypic heterogeneity describes the occurrence of "nonconformist" cells within an isogenic population. The nonconformists show an expression profile partially different from that of the remainder of the population. Phenotypic heterogeneity affects many aspects of the different bacterial lifestyles, and it is assumed that it increases bacterial fitness and the chances for survival of the whole population or smaller subpopulations in unfavorable environments. Well-known examples for phenotypic heterogeneity have been associated with antibiotic resistance and frequently occurring persister cells. Other examples include heterogeneous behavior within biofilms, DNA uptake and bacterial competence, motility (i.e., the synthesis of additional flagella), onset of spore formation, lysis of phages within a small subpopulation, and others. Interestingly, phenotypic heterogeneity was recently also observed with respect to quorum-sensing (QS)-dependent processes, and the expression of autoinducer (AI) synthase genes and other QS-dependent genes was found to be highly heterogeneous at a single-cell level. This phenomenon was observed in several Gram-negative bacteria affiliated with the genera Vibrio, Dinoroseobacter, Pseudomonas, Sinorhizobium, and Mesorhizobium. A similar observation was made for the Gram-positive bacterium Listeria monocytogenes. Since AI molecules have historically been thought to be the keys to homogeneous behavior within isogenic populations, the observation of heterogeneous expression is quite intriguing and adds a new level of complexity to the QS-dependent regulatory networks. All together, the many examples of phenotypic heterogeneity imply that we may have to partially revise the concept of homogeneous and coordinated gene expression in isogenic bacterial populations. Bacteria have evolved multiple strategies to cope with rapid and frequent changes in their environment. These survival strategies may include spore formation, increased production of polysaccharides, biofilm formation or escape from biofilms (i.e., switching from a motile into a sessile form and vice versa), altered motility, change of metabolic capabilities, response to antibiotics, and many more. In general, these switches are initiated by environmental or bacterially produced signals that are perceived by a diverse array of regulators and delegated into the corresponding regulatory networks. This presumably results in altered transcription levels of different genes or operons, which eventually causes a change in the phenotype and a response to the environmental stimulus. Within this context, it is generally assumed that the majority of a population will undergo this switch within a short time period and that the population will show a mostly homogeneous expression profile. During the last decade, it became, however, evident that a certain fraction of cells in an isogenic population behaves differently from the others, even though the environment may not have changed significantly. The term "phenotypic heterogeneity" thereby descr...

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Section: Bacterial Qs: a System Thought To Coordinate Cells Instead Osupporting

confidence: 58%

“…Another interesting aspect of AI-linked heterogeneity was recently identified in the alphaproteobacterium Dinoroseobacter shibae (25). D. shibae is a member of the Roseobacter clade, which is highly abundant in marine habitats (26).…”

Section: Bacterial Qs: a System Thought To Coordinate Cells Instead Omentioning

confidence: 99%

Phenotypic Heterogeneity, a Phenomenon That May Explain Why Quorum Sensing Does Not Always Result in Truly Homogenous Cell Behavior

Grote

Krysciak

Streit

2015

Appl Environ Microbiol

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“…Recently we found that knock-out of the autoinducer synthase luxI 1 led to a reduced expression of ctrA , cckA , chpT, divL as well as the QS genes luxR 2 I 2 and the AHL synthase luxI 3 during exponential growth and stationary phase, resulting in a complete loss of autoinducer biosynthesis [27]. Here, we found that the latter QS genes were also down-regulated in the CtrA phosphorelay mutants in both growth phases (Figure 5B).…”

Section: Resultsmentioning

confidence: 99%

The CtrA phosphorelay integrates differentiation and communication in the marine alphaproteobacterium Dinoroseobacter shibae

et al. 2014

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BackgroundDinoroseobacter shibae, a member of the Roseobacter clade abundant in marine environments, maintains morphological heterogeneity throughout growth, with small cells dividing by binary fission and large cells dividing by budding from one or both cell poles. This morphological heterogeneity is lost if the quorum sensing (QS) system is silenced, concurrent with a decreased expression of the CtrA phosphorelay, a regulatory system conserved in Alphaproteobacteria and the master regulator of the Caulobacter crescentus cell cycle. It consists of the sensor histidine kinase CckA, the phosphotransferase ChpT and the transcriptional regulator CtrA. Here we tested if the QS induced differentiation of D. shibae is mediated by the CtrA phosphorelay.ResultsMutants for ctrA, chpT and cckA showed almost homogeneous cell morphology and divided by binary fission. For ctrA and chpT, expression in trans on a plasmid caused the fraction of cells containing more than two chromosome equivalents to increase above wild-type level, indicating that gene copy number directly controls chromosome number. Transcriptome analysis revealed that CtrA is a master regulator for flagellar biosynthesis and has a great influence on the transition to stationary phase. Interestingly, the expression of the autoinducer synthase genes luxI2 and luxI3 was strongly reduced in all three mutants, resulting in loss of biosynthesis of acylated homoserine-lactones with C14 side-chain, but could be restored by expressing these genes in trans. Several phylogenetic clusters of Alphaproteobacteria revealed a CtrA binding site in the promoters of QS genes, including Roseobacters and Rhizobia.ConclusionsThe CtrA phosphorelay induces differentiation of a marine Roseobacter strain that is strikingly different from that of C. crescentus. Instead of a tightly regulated cell cycle and a switch between two morphotypes, the morphology and cell division of Dinoroseobacter shibae are highly heterogeneous. We discovered for the first time that the CtrA phosphorelay controls the biosynthesis of signaling molecules. Thus cell-cell communication and differentiation are interlinked in this organism. This may be a common strategy, since we found a similar genetic set-up in other species in the ecologically relevant group of Alphaproteobacteria. D. shibae will be a valuable model organism to study bacterial differentiation into pleomorphic cells.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-130) contains supplementary material, which is available to authorized users.

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“…are also known to possess multiple systems and signals ( Table 2). The QS signals modulating these QSS range from unsubstituted-to substituted-HSLs, as well as peptides (DKPs), quinolones, hormones [69,[94][95][96][97][98][99][100][101][102][103][104][105]. In Yersinia, luxI/R homologues are majorly regulated by substituted AHLs [106][107][108].…”

Section: Othersmentioning

confidence: 99%

Potential Emergence of Multi-quorum Sensing Inhibitor Resistant (MQSIR) Bacteria

et al. 2015

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Expression of certain bacterial genes only at a high bacterial cell density is termed as quorum-sensing (QS). Here bacteria use signaling molecules to communicate among themselves. QS mediated genes are generally involved in the expression of phenotypes such as bioluminescence, biofilm formation, competence, nodulation, and virulence. QS systems (QSS) vary from a single in Vibrio spp. to multiple in Pseudomonas and Sinorhizobium species. The complexity of QSS is further enhanced by the multiplicity of signals: (1) peptides, (2) acyl-homoserine lactones, (3) diketopiperazines. To counteract this pathogenic behaviour, a wide range of bioactive molecules acting as QS inhibitors (QSIs) have been elucidated. Unlike antibiotics, QSIs don't kill bacteria and act at much lower concentration than those of antibiotics. Bacterial ability to evolve resistance against multiple drugs has cautioned researchers to develop QSIs which may not generate undue pressure on bacteria to develop resistance against them. In this paper, we have discussed the implications of the diversity and multiplicity of QSS, in acting as an arsenal to withstand attack from QSIs and may use these as reservoirs to develop multi-QSI resistance.

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You are what you talk: quorum sensing induces individual morphologies and cell division modes in Dinoroseobacter shibae

Cited by 67 publications

References 66 publications

Phenotypic Heterogeneity, a Phenomenon That May Explain Why Quorum Sensing Does Not Always Result in Truly Homogenous Cell Behavior

Phenotypic Heterogeneity, a Phenomenon That May Explain Why Quorum Sensing Does Not Always Result in Truly Homogenous Cell Behavior

The CtrA phosphorelay integrates differentiation and communication in the marine alphaproteobacterium Dinoroseobacter shibae

Potential Emergence of Multi-quorum Sensing Inhibitor Resistant (MQSIR) Bacteria

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