Absence of Curli in Soil-Persistent Escherichia coli Is Mediated by a C-di-GMP Signaling Defect and Suggests Evidence of Biofilm-Independent Niche Specialization.

Yinka M Somorin,Leighton Pritchard,Fiona Brennan,Tara Vollmerhausen,Florence Abram,Nicholas Waters,Conor O’Byrne

doi:10.3389/fmicb.2018.01340

Abstract

Escherichia coli is commonly viewed as a gastrointestinal commensal or pathogen although an increasing body of evidence suggests that it can persist in non-host environments as well. Curli are a major component of biofilm in many enteric bacteria including E. coli and are important for adherence to different biotic and abiotic surfaces. In this study we investigated curli production in a unique collection of soil-persistent E. coli isolates and examined the role of curli formation in environmental persistence. Although most soil-persistent E. coli were curli-positive, 10% of isolates were curli-negative (17 out of 170). Curli-producing E. coli (COB583, COB585, and BW25113) displayed significantly more attachment to quartz sand than the curli-negative strains. Long-term soil survival experiments indicated that curli production was not required for long-term survival in live soil (over 110 days), as a curli-negative mutant BW25113ΔcsgB had similar survival compared to wild type BW25113. Mutations in two genes associated with c-di-GMP metabolism, dgcE and pdeR, correlated with loss of curli in eight soil-persistent strains, although this did not significantly impair their survival in soil compared to curli-positive strains. Overall, the data indicate that curli-deficient and biofilm-defective strains, that also have a defect in attachment to quartz sand, are able to reside in soil for long periods of time thus pointing to the possibility that niches may exist in the soil that can support long-term survival independently of biofilm formation.

Highlights

Escherichia coli is commonly associated with the gastrointestinal tract of humans, warm-blooded animals, and reptiles (Berg, 1996; Gordon and Cowling, 2003), and its presence in the external environment is often used as an indication of recent fecal contamination
Human commensal E. coli isolates, SE11 and SE15, were used for comparison purposes and both stained red on Congo Red (CR)-yeast extract and Casamino acid agar (YESCA) agar indicating curli production
E. coli BW25113, which was used as the positive control, was red while the negative control, E. coli BW25113 csgA, was white, confirming that the red staining was dependent on curli production

Summary

Introduction

Escherichia coli is commonly associated with the gastrointestinal tract of humans, warm-blooded animals, and reptiles (Berg, 1996; Gordon and Cowling, 2003), and its presence in the external environment is often used as an indication of recent fecal contamination. This niche specificity underpins its use as an indicator of fecal contamination in the environment. Brennan et al (2010) reported that E. coli are capable of long-term colonization and persistence in an lysimeters that had not been exposed to fecal material during a 10-year period prior to their isolation. When E. coli enters the soil, there is rapid decline in the population, but a part of the population is able to persist due to inherent physiological properties or has an ability to colonize favorable niches in the environment (Ogden et al, 2001)

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