Stress survival islet 1 contributes to serotype-specific differences in biofilm formation in Listeria monocytogenes

Abstract

Listeria monocytogenes has a significant impact on the food industry by forming biofilms on food-processing equipment. Tandem analysis of whole-genome sequencing data with biofilm data from 166 environmental and food-related L. monocytogenes isolates has revealed serotypic and genetic factors that strongly correlate with adherence and biofilm formation, such as lineage, plasmid harbourage, a three-codon deletion in inlA and the presence of the stress survival islet 1 (SSI-1). Strains from serotype 1/2b, the majority of which contained SSI-1, formed the strongest biofilms, while serotype 4b strains, the majority of which did not contain SSI-1, formed the weakest biofilms. When serotype 1/2a was separated by its SSI-1 genotype, SSI-1-positive 1/2a strains demonstrated significantly higher capacity for biofilm formation after 3 days of growth at 30°C (P < 0·0001). Together, these findings indicate that SSI-1 may contribute to serotype-associated differences in the biofilm-forming capacity in L. monocytogenes. SIGNIFICANCE AND IMPACT OF THE STUDY: Parallel analysis of whole-genome sequences and serotype-specific data was performed to identify genetic markers that correlate with increased adherence and biofilm formation in L. monocytogenes. The analyses revealed the hitherto unrecognized role of SSI-1 in biofilm formation, contributing to deeper understanding of genetic factors that influence behaviour of the species in the food processing environment..

Hypo- and Hyper-Virulent Listeria monocytogenes Clones Persisting in Two Different Food Processing Plants of Central Italy

“…These findings were consistent with previous studies reporting that serogroup IVb strains demonstrated a lower capacity for biofilm formation and that CC9 and CC121 were able to make more biofilm than CC1 and CC2 [4,61]. Moreover, Keeney et al [61] reported that the presence of SSI-1 was strongly correlated with biofilm formation and according to Franciosa et al [15], the PMSC mutation in the inlA gene was associated with enhanced biofilm levels when compared to the wild type inlA. Further studies investigated at the same time the influence of SSI-1 and a truncated inlA protein, finding that they were both significantly associated with increased levels of biofilm [14].…”

“…Statistically significant differences were found in the biofilm production by different Lm serogroups (IIa, IIb and IVb), with serogroups IIa and IVb presenting the highest and lowest values respectively. These findings were consistent with previous studies reporting that serogroup IVb strains demonstrated a lower capacity for biofilm formation and that CC9 and CC121 were able to make more biofilm than CC1 and CC2 [4,61]. Moreover, Keeney et al [61] reported that the presence of SSI-1 was strongly correlated with biofilm formation and according to Franciosa et al [15], the PMSC mutation in the inlA gene was associated with enhanced biofilm levels when compared to the wild type inlA.…”

“…This may have contributed to the long-lasting colonization of clusters A and B and suggested a potential persistence also for cluster C and the outlier Lm_2270/Lm_2272. The CC1 singleton detected in Meat A as well as all the CC2 strains from Dairy B lacked an SSI, consistently with their belonging to serogroup IVb [61].…”

Evolution of Listeria monocytogenes in a Food Processing Plant Involves Limited Single-Nucleotide Substitutions but Considerable Diversification by Gain and Loss of Prophages

“…While our study showed that the previously reported stress survival islets 1 and 2 (SSI-1 and -2, respectively) were associated with clusters and subclusters, we were not able to identify clear growth or stress response phenotypes associated with the presence of these islets. SSI-1 was detected among all cluster 3 isolates; this islet has been suggested to contribute to growth under low pH (pH 4.8), high salt (7.5% NaCl), and a combination of both (pH 5.2 and 5% NaCl) (8) as well as to biofilm formation at 30°C (37) and salt-induced nisin resistance (38). While 34 of 42 isolates in this study harbored SSI-1, only 3 of 12 isolates from a cold-smoked processing facility in Ireland harbored this islet (39).…”

Biofilm growth by Listeria monocytogenes on stainless steel and expression of biofilm-related genes under stressing conditions

“…Several genes may regulate bio lm development, allowing bacterial survival under adverse environmental conditions (Keeney et al 2018). Despite being also probably related to L. monocytogenes pathogenicity, the molecular mechanisms responsible for the expression of bio lm related genes are not completely understood (Lemon et al 2007;Bonsaglia et al 2014;Nowak et al 2017).…”