Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1

Abstract

Shewanella oneidensis MR-1 is capable of forming highly structured surface-attached communities. By DNase I treatment, we demonstrated that extracellular DNA (eDNA) serves as a structural component in all stages of biofilm formation under static and hydrodynamic conditions. We determined whether eDNA is released through cell lysis mediated by the three prophages LambdaSo, MuSo1 and MuSo2 that are harbored in the genome of S. oneidensis MR-1. Mutant analyses and infection studies revealed that all three prophages may individually lead to cell lysis. However, only LambdaSo and MuSo2 form infectious phage particles. Phage release and cell lysis already occur during early stages of static incubation. A mutant devoid of the prophages was significantly less prone to lysis in pure culture. In addition, the phage-less mutant was severely impaired in biofilm formation through all stages of development, and three-dimensional growth occurred independently of eDNA as a structural component. Thus, we suggest that in S. oneidensis MR-1 prophage-mediated lysis results in the release of crucial biofilm-promoting factors, in particular eDNA.

Impact of Spontaneous Prophage Induction on the Fitness of Bacterial Populations and Host-Microbe Interactions

“…Spontaneous SV1-mediated cell lysis was shown to occur in S. pneumoniae, and, accordingly, deletion of the SV1 phage lysin led to a decrease in cell lysis, eDNA release, and biofilm formation (69). In S. oneidensis, three prophages, MuSo1, MuSo2, and LambdaSo, jointly affect lysis and eDNA release, and consequently, a mutant devoid of all three phages is severely impaired in all stages of biofilm formation (70). Recent studies on this species have demonstrated that environmental iron levels are an important factor involved in inducing expression of LambdaSo in a RecA-dependent fashion during biofilm formation (71).…”

Functional Specificity of Extracellular Nucleases of Shewanella oneidensis MR-1

“…Notably, eDNA is not only a valuable nutrient for Shewanella and other species (41). We have recently demonstrated the presence of significant amounts of eDNA in S. oneidensis MR-1 biofilms, which are thought to be released by prophage-induced cell lysis (23). We demonstrated that treatment with DNase I strongly decreases the ability of S. oneidensis MR-1 to attach to a surface initially and that the subsequent formation of 3-dimensional structures is severely affected.…”

Organic phosphorus in the aquatic environment

“…it is believed that prophages in the bacterial genome are important for biofilm development because of the release of extracellular DNA on cell lysis. [52] Other nucleotides (e.g. ATP, GTP and AMP) In addition to DNA and RNA several other nucleotides have been identified in aquatic environments (Fig.…”

“…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.…”