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Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes.

ABSTRACT: We report here the characterization of dispersal variants from microcolony-type biofilms of Serratia marcescens MG1. Biofilm formation proceeds through a reproducible process of attachment, aggregation, microcolony development, hollow colony formation, and dispersal. From the time when hollow colonies were observed in flow cell biofilms after 3 to 4 days, at least six different morphological colony variants were consistently isolated from the biofilm effluent. The timing and pattern of variant formation were found to follow a predictable sequence, where some variants, such as a smooth variant with a sticky colony texture (SSV), could be consistently isolated at the time when mature hollow colonies were observed, whereas a variant that produced copious amounts of capsular polysaccharide (SUMV) was always isolated at late stages of biofilm development and coincided with cell death and biofilm dispersal or sloughing. The morphological variants differed extensively from the wild type in attachment, biofilm formation, and cell ultrastructure properties. For example, SSV formed two- to threefold more biofilm biomass than the wild type in batch biofilm assays, despite having a similar growth rate and attachment capacity. Interestingly, the SUMV, and no other variants, was readily isolated from an established SSV biofilm, indicating that the SUMV is a second-generation genetic variant derived from SSV. Planktonic cultures showed significantly lower frequencies of variant formation than the biofilms (5.05 x 10(-8) versus 4.83 x 10(-6), respectively), suggesting that there is strong, diversifying selection occurring within biofilms and that biofilm dispersal involves phenotypic radiation with divergent phenotypes.

SUBMITTER: Koh KS

PROVIDER: S-EPMC1797207 | biostudies-literature | 2007 Jan

REPOSITORIES: biostudies-literature

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Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes.

Koh Kai Shyang KS Lam Kin Wai KW Alhede Morten M Queck Shu Yeong SY Labbate Maurizio M Kjelleberg Staffan S Rice Scott A SA

Journal of bacteriology 20061027 1

We report here the characterization of dispersal variants from microcolony-type biofilms of Serratia marcescens MG1. Biofilm formation proceeds through a reproducible process of attachment, aggregation, microcolony development, hollow colony formation, and dispersal. From the time when hollow colonies were observed in flow cell biofilms after 3 to 4 days, at least six different morphological colony variants were consistently isolated from the biofilm effluent. The timing and pattern of variant f ...[more]

PMID: 17071749

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Project description:Bacteria can quickly adapt to constantly changing environments through a number of mechanisms, including secretion of secondary metabolites, peptides, and proteins. Serratia marcescens, an emerging pathogen with growing clinical importance due to its intrinsic resistance to several classes of antibiotics, can cause an array of infections in immunocompromised individuals. To better control the spread of S. marcescens infections, it is critical to identify additional targets for bacterial growth inhibition. We found that extracellular metabolites produced by the wild-type organism in response to peroxide exposure had a protective effect on an otherwise-H2O2-sensitive ΔmacAB indicator strain. Detailed analysis of the conditioned medium demonstrated that the protective effect was associated with a low-molecular-weight heat-sensitive and proteinase K-sensitive metabolite. Furthermore, liquid chromatography-tandem mass spectrometry analysis of the low-molecular-weight proteins present in the conditioned medium led to identification of the previously uncharacterized DUF1471-containing protein TBU67220 (SrfN). We found that loss of the srfN gene did not have an impact on the production of extracellular enzymes. However, the S. marcescens mutant lacking SrfN was significantly more sensitive to growth in medium with a low pH and to exposure to oxidative stress. Both defects were fully rescued by complementation. Thus, our results indicate that SrfN, a low-molecular-weight DUF1471-containing protein, is involved in S. marcescens SM6 adaptation to adverse environmental conditions. IMPORTANCE Serratia marcescens is ubiquitous in the environment and can survive in water, soil, plants, insects, and animals, and it can also cause infections in humans. In the face of disturbances such as oxidative or low-pH stress, bacteria adapt, survive, and recover through several mechanisms, including changes in their secretome. We show that a hydrogen peroxide-exposed S. marcescens milieu contains a small previously uncharacterized DUF1471-containing protein similar to the SrfN protein in Salmonella enterica serovar Typhimurium, and we illustrate the role of this protein in bacterial survival during acid and oxidative stresses.

Project description:PrtA is the major secreted metalloprotease of Serratia marcescens Previous reports implicate PrtA in the pathogenic capacity of this bacterium. PrtA is also clinically used as a potent analgesic and anti-inflammatory drug, and its catalytic properties attract industrial interest. Comparatively, there is scarce knowledge about the mechanisms that physiologically govern PrtA expression in Serratia In this work, we demonstrate that PrtA production is derepressed when the bacterial growth temperature decreases from 37°C to 30°C. We show that this thermoregulation occurs at the transcriptional level. We determined that upstream of prtA, there is a conserved motif that is directly recognized by the CpxR transcriptional regulator. This feature is found along Serratia strains irrespective of their isolation source, suggesting an evolutionary conservation of CpxR-dependent regulation of PrtA expression. We found that in S. marcescens, the CpxAR system is more active at 37°C than at 30°C. In good agreement with these results, in a cpxR mutant background, prtA is derepressed at 37°C, while overexpression of the NlpE lipoprotein, a well-known CpxAR-inducing condition, inhibits PrtA expression, suggesting that the levels of the activated form of CpxR are increased at 37°C over those at 30°C. In addition, we establish that PrtA is involved in the ability of S. marcescens to develop biofilm. In accordance, CpxR influences the biofilm phenotype only when bacteria are grown at 37°C. In sum, our findings shed light on regulatory mechanisms that fine-tune PrtA expression and reveal a novel role for PrtA in the lifestyle of S. marcescensIMPORTANCE We demonstrate that S. marcescens metalloprotease PrtA expression is transcriptionally thermoregulated. While strongly activated below 30°C, its expression is downregulated at 37°C. We found that in S. marcescens, the CpxAR signal transduction system, which responds to envelope stress and bacterial surface adhesion, is activated at 37°C and able to downregulate PrtA expression by direct interaction of CpxR with a binding motif located upstream of the prtA gene. Moreover, we reveal that PrtA expression favors the ability of S. marcescens to develop biofilm, irrespective of the bacterial growth temperature. In this context, thermoregulation along with a highly conserved CpxR-dependent modulation mechanism gives clues about the relevance of PrtA as a factor implicated in the persistence of S. marcescens on abiotic surfaces and in bacterial host colonization capacity.

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Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes.

Publications

Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes.

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