Impact of oxidative stress defense on bacterial survival and morphological change in Campylobacter jejuni under aerobic conditions

Abstract

Campylobacter jejuni, a microaerophilic foodborne pathogen, inescapably faces high oxygen tension during its transmission to humans. Thus, the ability of C. jejuni to survive under oxygen-rich conditions may significantly impact C. jejuni viability in food and food safety as well. In this study, we investigated the impact of oxidative stress resistance on the survival of C. jejuni under aerobic conditions by examining three mutants defective in key antioxidant genes, including ahpC, katA, and sodB. All the three mutants exhibited growth reduction under aerobic conditions compared to the wild-type (WT), and the ahpC mutant showed the most significant growth defect. The CFU reduction in the mutants was recovered to the WT level by complementation. Higher levels of reactive oxygen species were accumulated in C. jejuni under aerobic conditions than microaerobic conditions, and supplementation of culture media with an antioxidant recovered the growth of C. jejuni. The levels of lipid peroxidation and protein oxidation were significantly increased in the mutants compared to WT. Additionally, the mutants exhibited different morphological changes under aerobic conditions. The ahpC and katA mutants developed coccoid morphology by aeration, whereas the sodB mutant established elongated cellular morphology. Compared to microaerobic conditions, interestingly, aerobic culture conditions substantially induced the formation of coccoidal cells, and antioxidant treatment reduced the emergence of coccoid forms under aerobic conditions. The ATP concentrations and PMA–qPCR analysis supported that oxidative stress is a factor that induces the development of a viable-but-non-culturable state in C. jejuni. The findings in this study clearly demonstrated that oxidative stress resistance plays an important role in the survival and morphological changes of C. jejuni under aerobic conditions.

Stimulation of biofilm formation by oxidative stress inCampylobacter jejuniunder aerobic conditions

“…Our recent study also demonstrated that aerobic conditions promoted the development of a viable-but-non-culturable (VBNC) state in C. jejuni. 30 Based on our previous report and findings in this study, aerobic conditions may stimulate sessile C. jejuni cells to develop biofilms and planktonic cells to enter the VBNC state. Either the formation of biofilms or the development of VBNC stage would significantly affect the survival of this microaerophilic pathogen under harsh oxygen-rich conditions.…”

Current Perspectives on Viable but Non-culturable State in Foodborne Pathogens

“…For example, E. coli O157:H7 VBNC cells were induced by low temperature on the surface of lettuce and spinach plants (Dinu and Bach, 2013) and by UV disinfection (Zhang et al, 2015). Campylobacter jejuni VBNC cells were observed under oxygen-rich (Oh et al, 2015) and low temperature conditions (Chaisowwong et al, 2012). The cells of L. monocytogenes entered a VBNC state within 24 h in the presence of potassium sorbate at pH 4.0 (Cunningham et al, 2009).…”

“…In general, the factors (physical and chemical) create worse bacteria growth conditions that may stress the bacterial cells into the VBNC state. The physical factors that induce the VBNC state of bacteria mainly include low/high temperature (Dinu and Bach, 2013), drying (Barron and Forsythe, 2007), irradiation (Zhang et al, 2015), oxidative stress (Oh et al, 2015), starvation (Lothigius et al, 2010), a pulsed electric field (Rowan, 2004), pulsed light and high pressure carbon dioxide (HPCD) (Feng et al, 2016). The chemical factors include food preservatives and disinfectants (Oliver, 2010; Ding et al, 2016).…”

Members of the family Campylobacteraceae: Campylobacter jejuni, Campylobacter coli

“…The VBNC state of C. jejuni cells, which are of a coccoid form, can be induced under oxygen-rich aerobic conditions (Oh et al, 2015). Thus, the ability of microaerophilic Campylobacter spp.…”

“…detection and subsequent subtyping is not practical, since viable but not culturable (VBNC) Campylobacter cells occur (Tholozan et al, 1999;Abulreesh et al, 2006;Bronowski et al, 2014;Oh et al, 2015). The coupling of PCR detection after enrichment to the culture-based method increases the work load but substantially shortens the time requirement for detection and confirmation of Campylobacter spp.…”