Abstract

Ctenophores, also known as comb jellies, live across extremely broad ranges of temperature and hydrostatic pressure in the ocean. Because various ctenophore lineages adapted independently to similar environmental conditions, Phylum Ctenophora is an ideal system for the study of protein adaptation to extreme environments in a comparative framework. We present such a study here, using a phylogenetically-informed method to compare sequences of four essential metabolic enzymes across gradients of habitat depth and temperature. This method predicts convergent adaptation to these environmental parameters at the amino acid level, providing a novel view of protein adaptation to extreme environments and demonstrating the power and relevance of phylogenetic comparison applied to multi-species transcriptomic datasets from early-diverging metazoa. Across all four enzymes analyzed, 46 amino acid sites were associated with depth-adaptation, 59 with temperature-adaptation, and 56 with both. Sites predicted to be depth- and temperature-adaptive occurred consistently near Rossmann fold cofactor binding motifs and disproportionately in solvent-exposed regions of the protein. These results suggest that the hydrophobic effect and ligand binding may mediate efficient enzyme function at different hydrostatic pressures and temperatures. Using predicted adaptive site maps, such mechanistic hypotheses can now be tested via mutagenesis.

Highlights

  • Organisms like ctenophores, cnidarians, and sponges are notable for having colonized a vast diversity of habitats

  • Because various ctenophore lineages adapted independently to similar environmental conditions, Phylum Ctenophora is an ideal system for the study of protein adaptation to extreme environments in a comparative framework

  • We present such a study here, using a phylogenetically-informed method to compare sequences of four essential metabolic enzymes across gradients of habitat depth and temperature. This method predicts convergent adaptation to these environmental parameters at the amino acid level, providing a novel view of protein adaptation to extreme environments and demonstrating the power and relevance of phylogenetic comparison applied to multi-species transcriptomic datasets from early-diverging metazoa

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Summary

Introduction

Cnidarians, and sponges are notable for having colonized a vast diversity of habitats. Ctenophores, for instance, can be found from the equator to polar seas and from sea level to over 7000 m deep. Since ctenophores tend to lack physical protection for their cells, much of their prodigious environmental adaptation is biochemical. As such, it implicates changes in certain vital proteins, such as metabolic “housekeeping” enzymes, whose performance is sensitive to the environment. It implicates changes in certain vital proteins, such as metabolic “housekeeping” enzymes, whose performance is sensitive to the environment These changes should in turn be traceable to organisms’ transcriptomes. Despite the growing abundance of transcriptomes available for early-diverging taxa from a wide variety of environments, techniques for correlating protein-coding sites to phenotypes in multi-species datasets remain underdeveloped

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