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Cross-tolerance and transcriptional shifts underlying abiotic stress in the seabird tick, Ixodes uriae

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Abstract

The seabird tick, Ixodes uriae, is a significant ectoparasite of penguins in Antarctica and of other seabirds, mainly in coastal, polar regions of the Northern and Southern hemispheres, but the tick’s distribution extends into more temperate regions as well. The expansive range of this tick suggests that it is exposed to a wide range of abiotic stresses, including dehydration, heat, and cold. To better understand how I. uriae responds to stress exposure, we examined cross-tolerance between dehydration and thermal stress based on survival analyses and used RNA-seq to monitor transcriptional responses to cold, heat, and dehydration. Slight dehydration improved cold, but not heat tolerance, whereas severe dehydration reduced subsequent thermal tolerance. Dehydration exposure prompted transcript-level shifts underlying protein metabolism, recovery from stress, and processes allowing subsequent rehydration by water vapor uptake. Both cold and heat stress yielded expression changes involved in cuticle modification. One gene increased in expression (enzyme P450) and one decreased (transcription factor Hairy) in response to all three stresses. This study provides the groundwork for assessing stress tolerance in this bipolar ectoparasite.

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Data availability

All datasets used for RNA-seq analyses are available under the NCBI Bioproject PRJNA659796.

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Acknowledgements

This research was supported by the National Science Foundation grant DEB-1654417 (partially), United States Department of Agriculture 2018-67013-28495 (partially), and National Institutes of Health 1R01AI148551-01A1 (partially) to J.B.B. for computational support, National Science Foundation grant OPP-1341393 to D.L.D., and National Science Foundation grant OPP-1341385 to R.E.L. We thank the staff at Palmer Station, Antarctica for assistance in logistics and experiments. We appreciate Karen D. McCoy and Jingze Liu for serving as reviewers and providing helpful comments on the manuscript.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA

    Benjamin Davies & Joshua B. Benoit

  2. Department of Biology, Mount St. Joseph University, Cincinnati, OH, USA

    Andrew J. Rosendale

  3. Department of Biology, Miami University, Oxford, OH, USA

    Richard E. Lee Jr.

  4. Department of Biology and Health Science, Hendrix College, Conway, AR, USA

    Josiah D. Gantz

  5. Departments of Entomology and Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, OH, USA

    David L. Denlinger

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  1. Benjamin Davies
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Contributions

This study was designed and conceived by J.B.B and A.J.R. The manuscript was written by B.D. and J.B.B. RNA-seq studies were conducted by A.J.R., B. D., and J.B.B. Physiological studies were conducted by J.D.G and J.B.B. Samples were collected by J.D.G., J.B.B., R.E.L., and D.L.D. Figures were prepared by B.D. and J.B.B. All authors were responsible for editing the manuscript and have approved publication.

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Correspondence to Joshua B. Benoit.

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Supplementary Information

Below is the link to the electronic supplementary material.

300_2021_2887_MOESM1_ESM.xlsx

Supplementary file1—Online Resource 1 - RNA-seq results for contigs with increased expression following dehydration exposure in Ixodes uriae. Expression values are in transcripts per million. RNA-seq datasets are available under the following NCBI Bioproject PRJNA659796. (XLSX 36 kb)

300_2021_2887_MOESM2_ESM.xlsx

Supplementary file2—Online Resource 2 - RNA-seq results for contigs with decreased expression following dehydration exposure in Ixodes uriae. Expression values are in transcripts per million. RNA-seq datasets are available under the following NCBI Bioproject PRJNA659796. (XLSX 47 kb)

300_2021_2887_MOESM3_ESM.xlsx

Supplementary file3—Online Resource 3 - RNA-seq results for contigs with increased expression following cold exposure in Ixodes uriae. Expression values are in transcripts per million. RNA-seq datasets are available under the following NCBI Bioproject PRJNA659796. (XLSX 15 kb)

300_2021_2887_MOESM4_ESM.xlsx

Supplementary file4—Online Resource 4 - RNA-seq results for contigs with decreased expression following cold exposure in Ixodes uriae. Expression values are in transcripts per million. RNA-seq datasets are available under the following NCBI Bioproject PRJNA659796. (XLSX 16 kb)

300_2021_2887_MOESM5_ESM.xlsx

Supplementary file5—Online Resource 5 - RNA-seq results for contigs with increased expression following heat exposure in Ixodes uriae. Expression values are in transcripts per million. RNA-seq datasets are available under the following NCBI Bioproject PRJNA659796. (XLSX 16 kb)

300_2021_2887_MOESM6_ESM.xlsx

Supplementary file6—Online Resource 6 - RNA-seq results for contigs with decreased expression following heat exposure in Ixodes uriae. Expression values are in transcripts per million. RNA-seq datasets are available under the following NCBI Bioproject PRJNA659796. (XLSX 31 kb)

300_2021_2887_MOESM7_ESM.xlsx

Supplementary file7—Online Resource 7 - Gene ontology categories enriched following cold, heat, and dehydration exposure in Ixodes uriae. (XLSX 16 kb)

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Davies, B., Rosendale, A.J., Gantz, J.D. et al. Cross-tolerance and transcriptional shifts underlying abiotic stress in the seabird tick, Ixodes uriae. Polar Biol 44, 1379–1389 (2021). https://doi.org/10.1007/s00300-021-02887-4

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