Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut

Abstract

In addition to circulating haemocytes, the immune system of the solitary ascidian Ciona robusta relies on two organs, the pharynx and the gut, and encompasses a wide array of immune and stress-related genes. How the pharynx and the gut of C. robusta react and adapt to environmental stress was assessed upon short or long exposure to hypoxia/starvation in the absence or in the presence of polystyrene nanoplastics. We show that the immune response to stress is very different between the two organs, suggesting an organ-specific immune adaptation to the environmental changes. Notably, the presence of nanoplastics appears to alter the gene modulation induced by hypoxia/starvation in both organs, resulting in a partial increase in gene up-regulation in the pharynx and a less evident response to stress in the gut. We have also assessed whether the hypoxia/starvation stress could induce innate memory, measured as gene expression in response to a subsequent challenge with the bacterial agent LPS. Exposure to stress one week before challenge induced a substantial change in the response to LPS, with a general decrease of gene expression in the pharynx and a strong increase in the gut. Co-exposure with nanoplastics only partially modulated the stress-induced memory response to LPS, without substantially changing the stress-dependent gene expression profile in either organ. Overall, the presence of nanoplastics in the marine environment seems able to decrease the immune response of C. robusta to stressful conditions, hypothetically implying a reduced capacity to adapt to environmental changes, but only partially affects the stress-dependent induction of innate memory and subsequent responses to infectious challenges.

Context-dependent antioxidant defense system (ADS)-based stress memory in response to recurrent environmental challenges in congeneric invasive species

“…These findings underscore that C. robusta developed transcriptional stress memory from the earlier stress, supporting the notion of species-specific transcriptional stress memory. A similar phenomenon was reported in C. robusta : pre-exposure to Lipopolysaccharide (LPS) enhanced the transcriptional response of antioxidative-related genes in the gut (e.g., Cu/ZnSOD and GST) during later hypoxia/starvation (H/S) stresses (Marino et al 2023 ). The regulation of the ADS-related signaling pathway is critical for increasing the antioxidant capacity and membrane stability, which, in turn, reduces levels of malonaldehyde and the production of superoxide radicals.…”

Prophages regulateShewanella fidelis3313 motility and biofilm formation: implications for gut colonization dynamics inCiona robusta

“…To determine if host immunity discriminates among S. fidelis 3313 strains differing only in the presence or absence of prophages, we examined the expression patterns of immune-related genes, such as interleukin-17 and IL17 receptor, complement component 3a (C3a) receptor, NFκ−B, tumor necrosis factor alpha (TNFα), and mannose-binding lectin (MBL) [84]. We also tested VCBP-C, a secreted immune effector expressed in the gut epithelium of Ciona [85], can bind (and opsonize) bacteria within the gut lumen [42], and influence biofilms in vitro [43].…”

Stress Granule-Related Genes during Embryogenesis of an Invertebrate Chordate

“…This is especially true for organisms living in very variable environmental conditions, such as lagoons, marinas, or harbors. Recent studies have confirmed the ability of ascidians (sessile species of tunicates, the sister group of vertebrates) to cope with stressful conditions through the activation of both antioxidant (Franchi et al, 2012; Ferro et al, 2018) and immune responses (Parrinello et al, 2015; Franchi and Ballarin, 2017; Peronato et al, 2020; Marino et al, 2023). These responses are mainly detectable in hemocytes, representing the detoxification system of ascidians (Franchi et al, 2011, 2014).…”