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Research article
Francois Seneca
Centre Scientifique de Monaco
Corresponding Author
ORCiD: https://orcid.org/0000-0002-8908-1227
License:
This work is licensed under a CC BY 4.0 License. Read Full License
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.
Keywords
innate immunity, bacteria, infection, transcriptomics, Cnidaria
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This is a list of supplementary files associated with this preprint. Click to download.
- SuppFILE1TrinityRNASeqcommands.txt
- SuppTABLE1Percentagemappingforms.pdf
- SuppTABLE2FETstatsmastertable.xlsx
- SuppTABLE3Clustersannot.xlsx
- SuppTABLE4ImmunityDECsfulltable.xlsx
- SuppTABLE5ApoptosisDECsfulltable.xlsx
- SuppTABLE6DECsrelatedtoimmuneresponsesforms.pdf
- SuppTABLE7DECsrelatedtoapoptosiscascadesforms.pdf
- SuppTABLE83h6h12hLPSmastergenetable.xlsx
- SuppFIG1Aiptrescuepicsformssmall.jpg
- SuppFIG2ImmunityclassCateGOrizerforms.pdf
- SuppFIG3AVenndiagramseriesUPregulatedpanelA.pdf
- SuppFIG3BVenndiagramseriesDOWNregulatedpanelB.pdf
- SuppFIG4FETforDOWNDECs.pdf
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CURRENT STATUS: Published
View the published article at BMC Genomics.
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Editorial decision: Accept
On 09 Oct, 2020
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On 07 Oct, 2020
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On 06 Oct, 2020
Editor invited
On 06 Oct, 2020
Version 2
Posted 21 Sep, 2020
No comments provided
Editorial decision: Minor revision
On 02 Oct, 2020
Editor assigned
On 16 Sep, 2020
Submission checks complete
On 15 Sep, 2020
Editor invited
On 15 Sep, 2020
No comments provided
Review #2 received
Received 15 Jun, 2020
Editorial decision: Major revision
On 15 Jun, 2020
Review #1 received
Received 08 Jun, 2020
Reviewer #2 agreed
On 25 May, 2020
Reviewer #1 agreed
On 14 May, 2020
Reviewers invited
Invitations sent on 14 May, 2020
Editor assigned
On 23 Apr, 2020
Submission checks complete
On 22 Apr, 2020
Editor invited
On 22 Apr, 2020
First submitted
On 21 Apr, 2020
Version (no preprint)
Posted 08 May, 2020
Editorial decision: Minor revision
On 09 Sep, 2020
Editor assigned
On 25 Aug, 2020
Submission checks complete
On 24 Aug, 2020
Editor invited
On 24 Aug, 2020
This version was not preprinted
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A new preprint design is coming!
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See the published version of this preprint at BMC Genomics.
This is a preprint, a preliminary version of a manuscript that has not completed peer review at a journal. Research Square does not conduct peer review prior to posting preprints. The posting of a preprint on this server should not be interpreted as an endorsement of its validity or suitability for dissemination as established information or for guiding clinical practice.
Learn more about In Review
Research article
Francois Seneca
Centre Scientifique de Monaco
Corresponding Author
ORCiD: https://orcid.org/0000-0002-8908-1227
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
Prescreen
Peer Review Timeline
CURRENT STATUS: Published
View the published article at BMC Genomics.
No community comments so far
Editorial decision: Accept
On 09 Oct, 2020
Editor assigned
On 07 Oct, 2020
Submission checks complete
On 06 Oct, 2020
Editor invited
On 06 Oct, 2020
Version 2
Posted 21 Sep, 2020
No comments provided
Editorial decision: Minor revision
On 02 Oct, 2020
Editor assigned
On 16 Sep, 2020
Submission checks complete
On 15 Sep, 2020
Editor invited
On 15 Sep, 2020
No comments provided
Review #2 received
Received 15 Jun, 2020
Editorial decision: Major revision
On 15 Jun, 2020
Review #1 received
Received 08 Jun, 2020
Reviewer #2 agreed
On 25 May, 2020
Reviewer #1 agreed
On 14 May, 2020
Reviewers invited
Invitations sent on 14 May, 2020
Editor assigned
On 23 Apr, 2020
Submission checks complete
On 22 Apr, 2020
Editor invited
On 22 Apr, 2020
First submitted
On 21 Apr, 2020
Version (no preprint)
Posted 08 May, 2020
Editorial decision: Minor revision
On 09 Sep, 2020
Editor assigned
On 25 Aug, 2020
Submission checks complete
On 24 Aug, 2020
Editor invited
On 24 Aug, 2020
This version was not preprinted
Metrics
Comments: 0
PDF Downloads: ...
HTML Views: ...
Subject Areas
Epigenetics & Genomics
License:
This work is licensed under a CC BY 4.0 License. Read Full License
View the published article at BMC Genomics.
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.
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
This is a list of supplementary files associated with this preprint. Click to download.
- SuppFILE1TrinityRNASeqcommands.txt
- SuppTABLE1Percentagemappingforms.pdf
- SuppTABLE2FETstatsmastertable.xlsx
- SuppTABLE3Clustersannot.xlsx
- SuppTABLE4ImmunityDECsfulltable.xlsx
- SuppTABLE5ApoptosisDECsfulltable.xlsx
- SuppTABLE6DECsrelatedtoimmuneresponsesforms.pdf
- SuppTABLE7DECsrelatedtoapoptosiscascadesforms.pdf
- SuppTABLE83h6h12hLPSmastergenetable.xlsx
- SuppFIG1Aiptrescuepicsformssmall.jpg
- SuppFIG2ImmunityclassCateGOrizerforms.pdf
- SuppFIG3AVenndiagramseriesUPregulatedpanelA.pdf
- SuppFIG3BVenndiagramseriesDOWNregulatedpanelB.pdf
- SuppFIG4FETforDOWNDECs.pdf
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