Red Seaweeds Sarcodiotheca gaudichaudii and Chondrus crispus down Regulate Virulence Factors of Salmonella Enteritidis and Induce Immune Responses in Caenorhabditis elegans

Abstract

Red seaweeds are a rich source of unique bioactive compounds and secondary metabolites that are known to improve human and animal health. S. Enteritidis is a broad range host pathogen, which contaminates chicken and poultry products that end into the human food chain. Worldwide, Salmonella outbreaks have become an important economic and public health concern. Moreover, the development of resistance in Salmonella serovars toward multiple drugs highlights the need for alternative control strategies. This study evaluated the antimicrobial property of red seaweeds extracts against Salmonella Enteritidis using the Caenorhabditis elegans infection model. Six red seaweed species were tested for their antimicrobial activity against S. Enteritidis and two, Sarcodiotheca gaudichaudii (SG) and Chondrus crispus (CC), were found to exhibit such properties. Spread plate assay revealed that SG and CC (1%, w/v) significantly reduced the growth of S. Enteritidis. Seaweed water extracts (SWE) of SG and CC, at concentrations from 0.4 to 2 mg/ml, significantly reduced the growth of S. Enteritidis (log CFU 4.5–5.3 and log 5.7–6.0, respectively). However, methanolic extracts of CC and SG did not affect the growth of S. Enteritidis. Addition of SWE (0.2 mg/ml, CC and SG) significantly decreased biofilm formation and reduced the motility of S. Enteritidis. Quantitative real-time PCR analyses showed that SWE (CC and SG) suppressed the expression of quorum sensing gene sdiA and of Salmonella Pathogenesis Island-1 (SPI-1) associated genes sipA and invF, indicating that SWE might reduce the invasion of S. Enteritidis in the host by attenuating virulence factors. Furthermore, CC and SG water extracts significantly improved the survival of infected C. elegans by impairing the ability of S. Enteritidis to colonize the digestive tract of the nematode and by enhancing the expression of C. elegans immune responsive genes. As the innate immune response pathways of C. elegans and mammals show a high degree of conservation, these results suggest that these SWE may also impart beneficial effects on animal and human health.

Feed Supplementation with Red Seaweeds, Chondrus crispus and Sarcodiotheca gaudichaudii, Reduce Salmonella Enteritidis in Laying Hens

“…Chondrus crispus supplemented feed was effective in reducing S. Enteritidis count in the excreta and contents of the ceca. This could be due to the ability of seaweed to block the initial attachment of bacteria to the epithelial cells by targeting the motility and virulence of S. Enteritidis (Kulshreshtha et al, 2016). Furthermore, none of the egg yolk samples were positive for S. Enteritidis in the trial.…”

Black sea cucumber (Holothuria atra Jaeger, 1833) rescues Pseudomonas aeruginosa-infected Caenorhabditis elegans via reduction of pathogen virulence factors and enhancement of host immunity

“…QS have been corroborated as one of the crucial factor responsible for host mortality in the C. elegans slow killing assay (Papaioannou et al, 2009). Elsewhere, a marine seaweed extract was reported to repress P. aeruginosa QS genes, leading to diminished production of virulence factors and survival of infected worms (Kulshreshtha et al, 2016). Future work should ascertain the capacities of H. atra metabolites in interfering with pivotal elements of the P. aeruginosa QS.…”

“…The diverse marine environment impose the selection of an array of metabolites produced by an immeasurable source of organisms (Molinski et al, 2009). Secondary metabolites with anti-infective properties against P. aeruginosa have been identified from numerous marine organisms including marine bacteria and seaweeds (Fatin et al, 2017; Kandasamy et al, 2012; Kulshreshtha et al, 2016; Liu et al, 2013; Naik et al, 2013; Papa et al, 2015). To date, the only published report of an anti-infective from marine invertebrates using the C. elegans platform is from a tropical mollusk (Kong et al, 2014).…”

Beyond Traditional Antimicrobials: A Caenorhabditis elegans Model for Discovery of Novel Anti-infectives

“…Furthermore, the protective effect of C. crispus extract was diminished in selected C. elegans mutants ( pmk-1 , daf-2 , daf-16 , or skn-1 ), implying that the effect from the host perspective is mediated via the highly conserved immune pathways. Likewise, concurrent virulence inhibitory and immunostimulatory effects have also been observed in other seaweed-related natural products, including Tasco ® , a commercially available animal feed supplement made from the brown seaweed Ascophyllum nodosum (Kandasamy et al, 2012) and another red seaweed species Sarcodiotheca gaudichaudii (Kulshreshtha et al, 2016). Both, S. gaudichaudii and C. crispus extracts disarmed the pathogenicity of Salmonella enteritidis by reducing biofilm formation, swimming and swarming motility and down-regulating expression of virulence and quorum sensing genes in S. enteritidis.…”

“…Both, S. gaudichaudii and C. crispus extracts disarmed the pathogenicity of Salmonella enteritidis by reducing biofilm formation, swimming and swarming motility and down-regulating expression of virulence and quorum sensing genes in S. enteritidis. These extracts also reduced the intestinal bacterial load in C. elegans by promoting the expression of host immune response genes encoding lectin-family, saponin-like and antibacterial proteins (Kulshreshtha et al, 2016). Whilst no direct evidence of seaweed extract exerting an immunomodulatory effect on animal infection-directed immune responses, is available, Luo et al (2015) demonstrated that seaweed polysaccharide was immunomodulatory in a cell-culture based assay as well as in a mouse tumor model.…”