Extracellular nucleases and extracellular DNA play important roles inVibrio choleraebiofilm formation

Abstract

SUMMARY Biofilms are a preferred mode of survival for many microorganisms including Vibrio cholerae, the causative agent of the severe secretory diarrheal disease cholera. The ability of the facultative human pathogen V. cholerae to form biofilms is a key factor for persistence in aquatic ecosystems and biofilms act as a source for new outbreaks. Thus, a better understanding of biofilm formation and transmission of V. cholerae is an important target to control the disease. So far the Vibrio exopolysaccharide was the only known constituent of the biofilm matrix. In this study we identify and characterize extracellular DNA as a component of the Vibrio biofilm matrix. Furthermore, we show that extracellular DNA is modulated and controlled by the two extracellular nucleases Dns and Xds. Our results indicate that extracellular DNA and the extracellular nucleases are involved in diverse processes including the development of a typical biofilm architecture, nutrient acquisition, detachment from biofilms and the colonization fitness of biofilm clumps after ingestion by the host. This study provides new insights into biofilm development and transmission of biofilm-derived V. cholerae.

Mini-review: Inhibition of biofouling by marine microorganisms

“…On the other hand, the ability to degrade acetylated hexose amines and polymers containing them is widespread in marine bacteria (Riemann & Azam 2002;Krediet et al 2009), but it is not yet known whether these N-acetyl-glycosaminidases have a role to play in biofilm dispersal. Furthermore, nucleic acids are becoming recognised as an important component of biofilms, including those formed by V. cholerae (Nijland et al 2010;Seper et al 2011). Self-produced and exogenous nucleases reduced biofilm formation by at least twofold (Kaplan 2009;Nijland et al 2010;Seper et al 2011).…”

“…Furthermore, nucleic acids are becoming recognised as an important component of biofilms, including those formed by V. cholerae (Nijland et al 2010;Seper et al 2011). Self-produced and exogenous nucleases reduced biofilm formation by at least twofold (Kaplan 2009;Nijland et al 2010;Seper et al 2011). Therefore, a better understanding of the enzymatic activities by which marine bacteria dislodge existing biofilms will likely have further applications in the medical field and probably also for industry (Kaplan 2009).…”

Organic phosphorus in the aquatic environment

“…DNA is an important structural component of the extracellular polymer matrix of biofilms. [51][52][53] For V. cholera extracellular DNA is implicated in the development of biofilm architecture, nutrient acquisition and biofilm detachment. [53] For Shewanella sp.…”

“…[51][52][53] For V. cholera extracellular DNA is implicated in the development of biofilm architecture, nutrient acquisition and biofilm detachment. [53] For Shewanella sp. it is believed that prophages in the bacterial genome are important for biofilm development because of the release of extracellular DNA on cell lysis.…”

Genetics of Natural Competence in Vibrio cholerae and other Vibrios

“…Although detectable in the periplasm when expressed in E. coli (30), Dns and Xds are likely primarily extracellular in V. cholerae with ComEA playing a role in preventing extracellular DNA degradation by sequestration of DNA in the periplasm (28,29,31). Interestingly, both Dns and Xds also alter biofilm formation consistent with a role for extracellular DNA in biofilm structure (32). In both Gram − and Gram + bacteria, ssDNA is ultimately the form that enters the cytoplasm via the ComEC channel, although this has not been experimentally validated for vibrios.…”