A conserved Toll-like receptor-to-NF-κB signaling pathway in the endangered coral Orbicella faveolata

Williams, Leah M.; Fuess, Lauren E.; Brennan, Joseph; Mansfield, Katelyn M.; Salas-Rodriguez, Erick; Welsh, Julianne; Awtry, Jake A.; Banic, Sarah; Chacko, Cecilia; Chezian, Aarthia; Dowers, Donovan; Estrada, Felicia; Hsieh, Yu‐Hsuan; Kang, Jiawen; Li, Wanwen; Malchiodi, Zoe X.; Malinowski, John; Matuszak, Sean J.; McTigue, Thomas; Mueller, David M.; Nguyen, Brian; Nguyen, Michelle; Nguyen, Phuong; Nguyen, Sinead; Njoku, Ndidi; Patel, Khusbu; Pellegrini, William R.; Pliakas, Tessa; Qadir, Deena; Ryan, Emma; Schiffer, Alex; Thiel, Amber; Yunes, Sarah A.; Spilios, Kathryn E.; C, Jorge H. Pinzón; Mydlarz, Laura D.; Gilmore, Thomas D.

doi:10.1016/j.dci.2017.10.016

Cited by 59 publications

(105 citation statements)

References 47 publications

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“…We identified significantly upregulated TLR 2 and TLR 6 genes which are important innate immune pattern recognition receptors (PRR) that identify gram-negative bacteria and fungi respectively [64, 65]. These receptors are important in initiating the Nuclear Factor Kappa Beta (NF-kB) transcription factor [66–68] that causes production of cytokines and AMPS [69–71]. While other components of the NF-kB pathway were not significantly differentially expressed in this study, they are present in the A. palmata genome [34] and have been functionally characterized in the coral Orbicella faveolata [68].…”

Section: Discussionmentioning

confidence: 99%

Innate immune gene expression inAcropora palmatais consistent despite variance in yearly disease events

Young

Serrano

Rosales

et al. 2020

Preprint

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Coral disease outbreaks are expected to increase in prevalence, frequency and severity due to climate change and other anthropogenic stressors. This is especially worrying for the Caribbean branching Acropora palmata which has already seen an 80% decrease in its coral cover, with this primarily due to disease. Despite the importance of this species, there has yet to be a characterization of its transcriptomic response to disease exposure. In this study we provide the first transcriptomic analysis of 12 A. palmata genotypes, and their symbiont Symbiodiniaceae, exposed to disease in 2016 and 2017. Year was the primary driver of sample variance for A. palmata and the Symbiodiniaceae. Lower expression of ribosomal genes in the coral, and higher expression of transmembrane ion transport genes in the Symbiodiniaceae indicate that the increased virulence in 2017 may have been due to a dysbiosis between the coral and Symbiodiniaceae. We also identified a conserved suite of innate immune genes responding to the disease challenge that was activated in both years. This included genes from the Toll-like receptor and lectin pathways, and antimicrobial peptides. Co-expression analysis identified a module positively correlated to disease exposure rich in innate immune genes, with D-amino acid oxidase, a gene implicated in phagocytosis and microbiome homeostasis, as the hub gene. The role of D-amino acid oxidase in coral immunity has not been characterized but holds potential as an important enzyme for responding to disease. Our results indicate that A. palmata mounts a similar immune response to disease exposure as other coral species previously studied, but with unique features that may be critical to the survival of this keystone Caribbean species.

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Section: Discussionmentioning

confidence: 99%

Innate immune gene expression inAcropora palmatais consistent despite variance in yearly disease events

Young

Serrano

Rosales

et al. 2020

Preprint

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“…Moreover, gene knocked down experiments by RNAi of either HyTRR-1 or HyLRR-2 reciprocally reduced the expression of the other gene, and the production of antimicrobial peptides (Bosch et al 2009). In the coral O. faveolata too, the mccTLR protein can interact with human MyD88 (Williams et al 2018), while MyD88-deficient Hydra were more susceptible to infection with the human pathogen Pseudomonas aeruginosa (Franzenburg et al 2012). Taken together, these reports support an ancestral role of TLRs and TLR-like to NF-κB signaling in response to bacterial stimuli in cnidarians.…”

Section: Discussionmentioning

confidence: 99%

“…When comparing the conserved components of the TLR to NF-κB pathway, Brennan and Gilmore (2018) show that the pathway's structure in Ap diverges slightly from that of Nv, Hv, or the three coral species under consideration, as no TLR, NEMO or IκB homologs could be identified. Moreover, recent studies have characterized and provided functional evidences that TLR-like and the key mediator MyD88 proteins can interact to activate the transcription factor NF-κB and certain aspects of the innate immune response in the coral Orbicella faveolata (Williams et al 2018), Nc (Brennan et al 2017), and Hv (Bosch et al 2009). Most recently, a study brought further support for the role of NF-κB in the symbiosis of Ap with Symbiodinium algae and its survival to bacterial infection .…”

Section: Introductionmentioning

confidence: 96%

“…This provides a set of models to study the evolution of innate immunity as it is known in vertebrates. In particular, studies focusing on the characterization of the TLR to NF-κB like pathway and protein activity of its components in Hydra(Bosch et al 2009;Franzenburg et al 2012),Nematostella(Wolenski et al 2011;Brennan et al 2017) and Orbicella faveolata(Williams et al 2018), reveal some functional conservation in response to immune challenges (discussed below). With this in mind, this study aimed to contribute information about the active molecular component of innate immunity towards bacterial pathogens in Aiptasia, in order to identify genes and pathways relevant to vertebrate and human health.…”

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Conserved gene reactivity revealed in cnidarian innate immunity during zoonotic infection

Seneca

Davtian

Boyer

et al. 2020

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Cnidarians - the most primitive tissue-forming animals - can get infected with pathogens, defend themselves and heal. Recent sequencing projects on cnidarians have unveiled a rich innate immunity gene repertoire but little is known about their involvement in the host’s response against live pathogens over time. Vibrio parahaemolyticus (Vp) is a zoonotic threat originating from the ocean, which causes pandemics, and economic struggle to society. Here, we advance our understanding of the innate immunity from the transcriptome-wide response of a basal marine metazoan to infection with Vp. The dynamic of the response was assessed in a time series experiment following the gene activity of the anemone Aiptasia pallida strain CC7 infected or not with the Vp clinical strain O3:K6 and compared to the gene expression profile under LPS treatment. ResultsRNA-sequencing, gene expression and functional analyses detected hundreds of genes responsive to the Vp infection after 1, 3, 6 and 12 hours, including very few shared with the response to LPS. Members of the NOD-like receptor, C-type lectin receptor, and RIG-I-like receptor PRR families were responsive to the infection, but none from the canonical TLR family. A TLR-like pathway represented by MyD88, TRAF6, NF-κB and AP-1 was actively regulated in response to the infection but not by LPS, suggesting an alternative PAMP-PRR trigger to this pathway. Other activated pathways involving TNFRs likely lead to apoptosis which was enzymatically confirmed. Recently proposed novel innate immune genes in actinarians including CniFLs and NGs showed positive expression to infection.Conclusions Several innovations consisting of: possible neofunctionalization, conservation of signaling pathways over conservation of particular key genes, and involvement of lineage-specific immunity genes, denote the innate immune response to live pathogen in Aiptasia. Transduction of immune signals through a TLR-like pathway is supported. Two TNFR pathways could possibly lead to an inflammatory response and apoptosis, which we suggest takes place to fend off bacterial infection in Aiptasia. These results reveal the anemone’s innate immunity genes responsive to bacterial infection as well as potential novel candidates for future evolutionary as well as functional studies.

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“…Puri ed LPS -a Gram-negative speci c endotoxin -has been used to induce a more controlled innate immune response in coral species (Fuess et al 2017(Fuess et al , 2016Kvennefors et al 2010;Williams et al 2017) [27][28][29] and in anemones (Detournay et al 2012; Perez and Weis 2006;Neubauer et al 2016;Brennan et al 2017) [12,[30][31][32]. For example, in the coral Acropora millepora, the expression of a lectin homolog dubbed Millectin was found to bind to pathogens and be activated under both LPS and peptidoglycan treatments (Kvennefors et al 2010).…”

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confidence: 99%

Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection

Seneca

Davtian

Boyer

et al. 2020

Preprint

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Background: Recent sequencing projects on early-diverging metazoans such as cnidarians, have unveiled a rich innate immunity gene repertoire; however, little is known about immunity gene regulation in the host’s early response against marine bacterial pathogens over time. Here, we used RNA-seq on the sea anemone Exaiptasia pallida (Ep) strain CC7 as a model to depict the innate immune response during the onset of infection with the marine pathogenic bacteria Vibrio parahaemolyticus (Vp) clinical strain O3:K6, and lipopolysaccharides (LPS) exposure. Pairwise and time series analyses identified the genes responsive to infection as well as the kinetics of innate immune genes over time. Comparisons between the responses to live Vp and purified LPS was then performed.Results: Gene expression and functional analyses detected hundreds to thousands of genes responsive to the Vp infection after 1, 3, 6 and 12 hours, including a few shared with the response to LPS. Our results bring to light the first indications that non-canonical cytoplasmic pattern recognition receptors (PRRs) such as NOD-like and RIG-I-like receptor homologs take part in the immune response of Ep. Over-expression of several members of the lectin-complement pathways in parallel with novel transmembrane and Ig containing ficolins (CniFLs) suggest an active defense against the pathogen. Although lacking typical Toll-like receptors (TLRs), Ep activates a TLR-like pathway including the up-regulation of MyD88, TRAF6, NF-κB and AP-1 genes, which are not induced under LPS treatment and therefore suggest an alternative ligand-to-PRR trigger. Two cytokine-dependent pathways involving Tumor necrosis factor receptors (TNFRs) and several other potential downstream signaling genes likely lead to inflammation and/or apoptosis. Finally, both the extrinsic and intrinsic apoptotic pathways were strongly supported by over-expression of effector and executioner genes.Conclusions: To our knowledge, this pioneering study is first to follow the kinetics of the innate immune response in a cnidarian during the onset of infection with a bacterial pathogen. Overall, our findings reveal the involvement of both novel immune gene candidates such as NLRs, RLRs and CniFLs, and previously identified TLR-like and apoptotic pathways in anthozoan innate immunity with a large amount of transcript-level evidence.

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A conserved Toll-like receptor-to-NF-κB signaling pathway in the endangered coral Orbicella faveolata

Cited by 59 publications

References 47 publications

Innate immune gene expression inAcropora palmatais consistent despite variance in yearly disease events

Innate immune gene expression inAcropora palmatais consistent despite variance in yearly disease events

Conserved gene reactivity revealed in cnidarian innate immunity during zoonotic infection

Gene expression kinetics of Exaiptasia pallida innate immune response to Vibrio parahaemolyticus infection

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