An indoor study of the combined effect of industrial pollution and turbulence events on the gut environment in a marine invertebrate

Liberti, Assunta; Bertocci, Iacopo; Pollet, Amandine; Musco, Luigi; Locascio, Annamaria; Ristoratore, Filomena; Sordino, Paolo

doi:10.1016/j.marenvres.2020.104950

Cited by 15 publications

(7 citation statements)

References 109 publications

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“…The basal expression of sixteen genes was examined in C. robusta . Genes were selected based on three criteria, immune-related genes that are already known to be involved in the Ciona immune responses ( C3-1 , C3ar , Il17-1 , Il17-2 , Il17r , Tnf , Tgfb , Lbp , Tlr-2 , Tlr13 , Cd36 ) ( 19 – 26 ), pharynx- and gut-specific genes involved in mucosal immunity ( VCBP-B and VCPB-C ) ( 27 ) and oxidative stress-related genes ( Sod-A , GST , GR ) ( 29 ). Gene expression was measured in the two organs that display immune reactivity, namely the pharynx and the gut.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2023

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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.

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Section: Resultsmentioning

confidence: 99%

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

et al. 2023

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“…Such differences suggest the stimulation of production of mucus by colonized micro-PS by the sea urchin’s digestive tract. The overproduction of mucus is recognized as a defensive response against stressors including pollutants, , and therefore, it could have facilitated the rapid egestion of colonized micro-PS by sea urchins. Our preliminary findings support future studies aimed to underline the interactions, even mechanical, that might occur between micro-PS and the sea urchin’s digestive system.…”

Section: Resultsmentioning

confidence: 99%

Impact of Microbial Colonization of Polystyrene Microbeads on the Toxicological Responses in the Sea Urchin Paracentrotus lividus

Murano

Donnarumma

Corsi

et al. 2021

Environ. Sci. Technol.

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The sea urchin Paracentrotus lividus (P. lividus) was exposed to either virgin or biofilm-covered polystyrene microbeads (micro-PS, 45 μm) in order to test the effect of microbial colonization on the uptake, biodistribution, and immune response. The biofilm was dominated by bacteria, as detected by scanning electron microscopy and 16S rRNA sequencing. A higher internalization rate of colonized micro-PS inside sea urchins compared to virgin ones was detected, suggesting a role of the plastisphere in the interaction. Colonized and virgin micro-PS showed the same biodistribution pattern by accumulating mainly in the digestive system with higher levels and faster egestion rates for the colonized. However, a significant increase of catalase and total antioxidant activity was observed only in the digestive system of colonized micro-PS-exposed individuals. Colonized micro-PS also induced a significant decrease in the number of coelomocytes with a significant increase in vibratile cells, compared to control and virgin micro-PS-exposed animals. Moreover, a general time-dependent increase in the red/white amoebocytes ratio and reactive oxygen species and a decrease in nitrogen ones were observed upon exposure to both colonized and virgin micro-PS. Overall, micro-PS colonization clearly affected the uptake and toxicological responses of the Mediterranean sea urchin P. lividus in comparison to virgin micro-PS.

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“…Mechanisms of adaptation to chronic exposure to chemical mixtures was also suggested, revealing that turbulence events inducing polluted sediment suspension and a consequent release of heavy metals and polycyclic aromatic hydrocarbons do not correlate with an antioxidant response in Ciona, but instead with a pro-inflammatory response, as suggested by the increase in gene expression of CiTNFa. On the contrary, the absence of effects on gene expression of molecules involved in the establishment and maintenance of barrier defenses, such as MUC, chitin synthases, and also VCBPs, suggested that the mixture of pollutants did not interfere with the host-microorganisms interaction in the gut (159). However, the availability of a more comprehensive multiomics approach would further help elucidate, utilizing high throughput and untargeted methods, the impact of environmental pollutants on the composition, behavior, or metabolic potential of gut microbial communities as well as to the predictive interpretations of the functional impacts on the animal host (155).…”

Section: Multi-omics Approaches In Ciona Model For Studies In Ecotoximentioning

confidence: 99%

“…Additionally, most of these studies have been performed in mammals; however, since most of the contaminants are released in aquatic environments, an important consideration is how aquatic organisms, which face continuous exposures, are impacted (17). A recent ecotoxicological investigation leveraged Ciona robusta as a model, assessing the impact of the combined effect of both industrial pollution (from the industrial area of Bagnoli-Coroglio, Naples, Italy) and two temporal patterns of turbulence events on the gut environment (159). Four broad categories were investigated: oxidative stress, innate immunity, host-microbial interactions, and integrity of gut epithelial barrier, with a focus on expression patterns of oxidative pathway and immune response genes (159).…”

Section: Multi-omics Approaches In Ciona Model For Studies In Ecotoximentioning

confidence: 99%

“…A recent ecotoxicological investigation leveraged Ciona robusta as a model, assessing the impact of the combined effect of both industrial pollution (from the industrial area of Bagnoli-Coroglio, Naples, Italy) and two temporal patterns of turbulence events on the gut environment (159). Four broad categories were investigated: oxidative stress, innate immunity, host-microbial interactions, and integrity of gut epithelial barrier, with a focus on expression patterns of oxidative pathway and immune response genes (159). In particular, evidence for the induction of antioxidant defenses was detected after 7 days of exposure to static, polluted, sediment, with higher levels of glutathione S-transferase and metallothionein gene expression observed.…”

Section: Multi-omics Approaches In Ciona Model For Studies In Ecotoximentioning

confidence: 99%

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Reflections on the Use of an Invertebrate Chordate Model System for Studies of Gut Microbial Immune Interactions

et al. 2021

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The functional ecology of the gastrointestinal tract impacts host physiology, and its dysregulation is at the center of various diseases. The immune system, and specifically innate immunity, plays a fundamental role in modulating the interface of host and microbes in the gut. While humans remain a primary focus of research in this field, the use of diverse model systems help inform us of the fundamental principles legislating homeostasis in the gut. Invertebrates, which lack vertebrate-style adaptive immunity, can help define conserved features of innate immunity that shape the gut ecosystem. In this context, we previously proposed the use of a marine invertebrate, the protochordate Ciona robusta, as a novel tractable model system for studies of host-microbiome interactions. Significant progress, reviewed herein, has been made to fulfill that vision. We examine and review discoveries from Ciona that include roles for a secreted immune effector interacting with elements of the microbiota, as well as chitin-rich mucus lining the gut epithelium, the gut-associated microbiome of adults, and the establishment of a large catalog of cultured isolates with which juveniles can be colonized. Also discussed is the establishment of methods to rear the animals germ-free, an essential technology for dissecting the symbiotic interactions at play. As the foundation is now set to extend these studies into the future, broadening our comprehension of how host effectors shape the ecology of these microbial communities in ways that establish and maintain homeostasis will require full utilization of “multi-omics” approaches to merge computational sciences, modeling, and experimental biology in hypothesis-driven investigations.

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An indoor study of the combined effect of industrial pollution and turbulence events on the gut environment in a marine invertebrate

Cited by 15 publications

References 109 publications

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

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

Impact of Microbial Colonization of Polystyrene Microbeads on the Toxicological Responses in the Sea Urchin Paracentrotus lividus

Reflections on the Use of an Invertebrate Chordate Model System for Studies of Gut Microbial Immune Interactions

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