Growing up gator: a proteomic perspective on cardiac maturation in an oviparous reptile, the American alligator (Alligator mississippiensis)

Abstract

We recently described lasting changes in the cardiac proteome of American alligators (Alligator mississippiensis) reared under hypoxic conditions, that resemble what embryos encounter in natural nests. While these changes were consistent with functional differences in cardiac performance induced by developmental hypoxia, the magnitude of this response was dwarfed by a much greater effect of development alone (76% of the total differentially abundant proteins). This means that substantial differences in relative steady-state protein expression occur in the hearts of alligators as they mature from egg-bound embryos to 2-year-old juveniles, and this developmental program is largely resistant to variation in nest conditions. We therefore performed functional enrichment analysis of the 412 DA proteins that were altered by development but not hypoxia, to gain insight into the mechanisms of cardiac maturation in this ectotherm. We found that the cardiac proteome of alligators at 90% of embryonic development retained a considerable capacity for transcription and translation, suggesting the heart was still primarily invested in growth even as the animal approached hatching. By contrast, the cardiac proteome of 2-year-old juveniles was weighted towards structural and energetic processes typical of a working heart. We discuss our results in the context of differences in cardiac development between ectothermic and endothermic oviparous vertebrates, and argue that the robust developmental program of the alligator heart reflects a slow-paced ontogeny, unburdened by the requirement to support the elevated peripheral oxygen demand typical of endothermic animals from a young age.

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Acknowledgements

We would like to acknowledge Derek Nelson, Justin Conner, Amanda Reynolds and Janna Crossley for their contribution to animal care. The authors wish to thank Jonathan Krieger of SPARC BioCentre Molecular Analysis, The Hospital for Sick Children, Toronto, Canada for assistance with iTRAQ analysis. D.A.C.II. is supported by a University of North Texas Office of Research and Innovation award and by a National Science Foundation CAREER award IBN IOS-0845741. T.E.G. is supported by a Natural Sciences and Engineering Research Council (NSERC) of Canada Discovery Grant (No. 71489) and an NSERC Discovery Accelerator Supplement.

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DACII, SLA, and TEG conceived the experiments; DACII and SLA conducted the experiments; SLA and TEG analyzed the results; RME provided alligator eggs. All authors reviewed the manuscript.

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Correspondence to Sarah L. Alderman.

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Alderman, S.L., Crossley, D.A., Elsey, R.M. et al. Growing up gator: a proteomic perspective on cardiac maturation in an oviparous reptile, the American alligator (Alligator mississippiensis). J Comp Physiol B 190, 243–252 (2020). https://doi.org/10.1007/s00360-020-01257-6

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Keywords

  • Heart
  • Reptile
  • Oxygen
  • iTRAQ
  • Developmental programming
  • Phenotypic plasticity