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Transcriptomic Variation of Amphiprion Percula (Lacepède, 1802) in Response to Infection with Cryptocaryon Irritans Brown, 1951

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Abstract

Cryptocaryon irritans (Brown 1951) frequently infect the Pomacentridae fishes causing severe economic losses. However, the anti-C. irritans’ molecular mechanism in these fishes remains largely unknown. To address this issue, we conducted RNA-Seq for C. irrtians-infected gills of the clownfish Amphiprion percula (Lacepède 1802) at the early (day 1) and late (day 3) stages of infection. A total of 1655 differentially expressed genes (DEGs) were identified. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses of DEGs showed a vast genetic variation related to the following aspects: ECM-receptor interaction, P13K-Akt signalling, cytokine-cytokine receptor interaction, and endocytosis. During the early phase of infection, key genes involved in ATP production, energy homeostasis, and stress control were abruptly increased. In the late phase, however, acute response molecules of the peripheral nervous system (synaptic transmission and local immunity), metabolic system triggering glycogen synthesis, energy maintenance, and osmoregulation were found to be critical. The highest number of upregulated genes (URGs) recovered during the early phase was included under the ‘biological process’ category, which primarily functions as response to stimuli, signalling, and biological regulation. In the late phase, most of the URGs were related to gene regulation and immune system processes under ‘molecular function’ category. The immune-related URGs of early infection include major histocompatibility complex (MHC) class-II molecules apparently triggering CD4+ T-cell–activated Th responses, and that of late infection include MHC class-1 molecules for the possible culmination of CD8+ T-cell triggered cytotoxicity. The high level of genic single nucleotide polymorphisms (SNPs) identified during the late phase of infection is likely to influence their susceptibility to secondary infection. In summary, the identified DEGs and their related metabolic and immune-related pathways and the SNPs may provide new insights into coordinating the immunological events and improving resistance in Pomacentridae fishes against C. irritans.

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Data Availability

The datasets generated during and/or analysed during the current study are available in the NCBI repository, [gene ID: PRJNA832516].

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Acknowledgements

We wish to thank M/s Eurofins Genomics India Pvt. Ltd., Bengaluru, for sequencing and bioinformatics support. We are very grateful to the Central University of Kerala for providing us the laboratory space and literature resources.

Funding

This study was supported by Department of Science and Technology, Government of India, DST WOS-A research project (No. SR/WOS-A/LS-78/2018 (G), 28.06.2019), DST-RFBR collaborative research project (No. INT/RUS/RFBR/P-330, 10.01.2019), and DST-SERB Research project (No. EMR/2016/001163/AS, 28.08. 2017).

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  1. Department of Zoology, School of Biological Sciences, Central University of Kerala, Kasaragod, 671316, India

    Jose Priya T. A., Charutha Karunakaran, Aishwarya Nath & Sudha Kappalli

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Contributions

Jose Priya TA conceived and designed the project, carried out the experiment, analysed data, and wrote the manuscript; Charutha Karunakaran contributed to sample collection and assisted with data processing; Aishwarya Nath discussed the results and contributed to the final manuscript; Sudha Kappalli did critical reading and editing. All authors read and approved the final version of the manuscript.

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Correspondence to Jose Priya T. A. or Sudha Kappalli.

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Highlights

• Infection with Cryptocaryon irritans resulted in a large number of DEGs in the gill tissue of Amphiprion percula.

• At the initial phase of infection, C. irritans induced significant responses on key genes involved in ATP production, energy homeostasis, stress control, and MHC-II-mediated immunity.

• At the late phase, acute responses of local immunity, glycogen metabolism, osmoregulation, and MHC-I-mediated immunity were induced.

• Single nucleotide polymorphisms (SNPs) were estimated to be 1.4-fold higher during the late phase of infection, revealing a higher probability of secondary infection.

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T. A., J., Karunakaran, C., Nath, A. et al. Transcriptomic Variation of Amphiprion Percula (Lacepède, 1802) in Response to Infection with Cryptocaryon Irritans Brown, 1951. Mar Biotechnol 25, 858–890 (2023). https://doi.org/10.1007/s10126-023-10246-z

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