Evolution of the immune system in Antarctic notothenioids

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Transcriptomic down-regulation of immune system components in barrier and hematopoietic tissues after lipopolysaccharide injection in antarctic notothenia coriiceps

Publication . Sousa, Carmen; Power, Deborah; Guerreiro, Pedro M; Louro, Bruno; Chen, Liangbiao; Canario, Adelino

The environmental conditions and isolation in the Antarctic have driven the evolution of a unique biodiversity at a macro to microorganism scale. Here, we investigated the possible adaptation of the teleost Notothenia coriiceps immune system to the cold environment and unique microbial community of the Southern Ocean. The fish immune system was stimulated through an intraperitoneal injection of lipopolysaccharide (LPS 0111:B4 from E. coli) and the tissue transcriptomic response and plasma biochemistry were analyzed 7 days later and compared to a sham injected control. Gene transcription in the head-kidney, intestine and skin was significantly modified by LPS, although tissues showed different responsiveness, with the duodenum most modified and the skin the least modified. The most modified processes in head-kidney, duodenum and skin were related to cell metabolism (up-regulated) and the immune system (comprising 30% of differentially expressed genes). The immune processes identified were mostly down-regulated, particularly interleukins and pattern recognition receptors (PRRs), nucleotide-binding oligomerization domain-like receptors and mannose receptors, unlike the toll-like receptors response commonly described in other teleost fish. The modified transcriptional response was not mirrored by a modified systemic response, as the circulating levels of enzymes of innate immunity, lysozyme and antiproteases, were not significantly different from the untreated and sham control fish. In conclusion, while the N. coriiceps immune system shares many features with other teleosts there are also some specificities. Further studies should better characterize the PRRs and their role in Antarctic teleosts, as well as the importance of the LPS source and its consequences for immune activation in teleosts.

2022-07-16Journal article

Open access

Toll-like receptor evolution: does temperature matter?

Publication . Sousa, Carmen; Fernandes, Stefan A.; Cardoso, João; Wang, Ying; Zhai, Wanying; Guerreiro, Pedro; Chen, Liangbiao; Canario, A.V.M.; Power, Deborah

Toll-like receptors (TLRs) recognize conserved pathogen-associated molecular patterns (PAMPs) and are an ancient and well-conserved group of pattern recognition receptors (PRRs). The isolation of the Antarctic continent and its unique teleost fish and microbiota prompted the present investigation into Tlr evolution. Gene homologues of tlr members in teleosts from temperate regions were present in the genome of Antarctic Nototheniidae and the non-Antarctic sister lineage Bovichtidae. Overall, in Nototheniidae apart from D. mawsoni, no major tlr gene family expansion or contraction occurred. Instead, lineage and species-specific changes in the ectodomain and LRR of Tlrs occurred, particularly in the Tlr11 superfamily that is well represented in fish. Positive selective pressure and associated sequence modifications in the TLR ectodomain and within the leucine-rich repeats (LRR), important for pathogen recognition, occurred in Tlr5, Tlr8, Tlr13, Tlr21, Tlr22, and Tlr23 presumably associated with the unique Antarctic microbiota. Exposure to lipopolysaccharide (Escherichia coli O111:B4) Gram negative bacteria did not modify tlr gene expression in N. rossii head-kidney or anterior intestine, although increased water temperature (+4 degrees C) had a significant effect.

2022-02Journal article

Open access

Evolution of the immune system in Antarctic notothenioids

Publication . Sousa, Cármen Sofia Vieira de; Canário, Adelino V. M.; Power, Deborah

Notothenioids are the most abundant group of teleost fish found in the Southern Ocean. These fish evolved relatively recently from a single benthic ancestor and radiated and expanded in the extreme cold of Antarctica waters and their physiology was adapted accordingly. Surprisingly, little is known about their immune system and how immune defences were modulated during adaptation to the cold environment and to its water specific microbiome. The main objective of this thesis was to characterise the immune cellular and humoral responses to bacterial and viral-like challenges in immune tissues and plasma of two phylogenetically related notothenioids, Notothenia coriiceps and Notothenia rossii. The methodologies applied were based on DNA sequencing technologies and biochemical assays to measure functional plasma enzyme activity using a comparative approach. This study a) characterised and uncovered a role of iron-metabolism and of the pattern recognition receptors family toll-like receptors (TLRs) after a LPS immune challenge, b) characterised for the first time the transcriptomes of important immune tissues (head-kidney, skin, duodenum, liver and spleen) and their response to bacterial and viral challenges and in response to temperature, c) described the microbiome communities associated to important immune tissue barriers in recently caught and immune challenged notothenioids. The results contribute substantially to the understanding of the main immune and non-immune pathways in the defence against external agents in Antarctic notothenioids.

2022-04-11Doctoral thesis

Open access