Himmel NJ et al. (2020), Phylogenetics Identifies Two Eumetazoan TRPM Cl...

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Mol Biol Evol 2020 Jul 01;377:2034-2044. doi: 10.1093/molbev/msaa065.

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Phylogenetics Identifies Two Eumetazoan TRPM Clades and an Eighth TRP Family, TRP Soromelastatin (TRPS).

Himmel NJ , Gray TR , Cox DN .

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Transient receptor potential melastatins (TRPMs) are most well known as cold and menthol sensors, but are in fact broadly critical for life, from ion homeostasis to reproduction. Yet, the evolutionary relationship between TRPM channels remains largely unresolved, particularly with respect to the placement of several highly divergent members. To characterize the evolution of TRPM and like channels, we performed a large-scale phylogenetic analysis of >1,300 TRPM-like sequences from 14 phyla (Annelida, Arthropoda, Brachiopoda, Chordata, Cnidaria, Echinodermata, Hemichordata, Mollusca, Nematoda, Nemertea, Phoronida, Priapulida, Tardigrada, and Xenacoelomorpha), including sequences from a variety of recently sequenced genomes that fill what would otherwise be substantial taxonomic gaps. These findings suggest: 1) the previously recognized TRPM family is in fact two distinct families, including canonical TRPM channels and an eighth major previously undescribed family of animal TRP channel, TRP soromelastatin; 2) two TRPM clades predate the last bilaterian-cnidarian ancestor; and 3) the vertebrate-centric trend of categorizing TRPM channels as 1-8 is inappropriate for most phyla, including other chordates.

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	Fig. 1. Major, widely recognized taxa included in these phylogenetic analyses and relationships assumed throughout. TRPM and TRPM-like sequences were collected for 318 species, from 14 diverse eumetazoan phyla (Annelida, Arthropoda, Brachiopoda, Chordata, Cnidaria, Echinodermata, Hemichordata, Mollusca, Nematoda, Nemertea, Phoronida, Priapulida, Tardigrada, and Xenacoelomorpha).
	Fig. 2. Caenorhabditis elegans ced-11, and ced-11-like sequences, belong to a previously unrecognized family of TRP channels, the TRPS. TRPM-like and ced-11-like sequences form two distinct clades, with the topology suggesting divergence prior to the Cnidaria–Bilateria split. (A) Maximum likelihood tree showing the relationship between traditional TRPM and TRPS/ced-11-like sequences among those species that have TRPS/ced-11-like species. Full annotated tree available in supplementary figure S1, Supplementary Material online; alternative hypothesis testing in supplementary figures S3 and S4, Supplementary Material online. (B) Left, summary of maximum likelihood analysis and branch support (UFboot) for indicated clades. Right, presence or absence of family in indicated taxa (where Bilateria is Xenacoelomorpha+Nephrozoa). Solid lines in color indicate that the TRP family is present in the indicated taxon, whereas dashed lines in gray indicate that no sequences were found for the indicated taxon. Family specific duplication/loss events summarized in figures 4 and 5.
	Fig. 3. TRPS and TRPM are, putatively, structurally and functionally distinct, and their domain arrangements suggest a SLOG- and Nudix-linked, ankyrin-free TRPS–TRPM ancestor. (A) Principal component analyses of pairwise sequence identity for alignment of TRPC, TRPN, TRPM, and ced-11-like (TRPS) sequences show four distinct clusters. 3D PCA plot extracted from Jalview and plotted in two transformed, arbitrary dimensions. PCA against just TM segments in supplementary figure S2, Supplementary Material online. (B) Like TRPM channels, these TRPS channels have both SLOG and Nudix domains, but lack the kinase domain associated with a small subset of TRPM channels. Moreover, these TRPS channels have a divergent consensus sequence in the highly conserved TRP domain. (C) In Caenorhabditis elegans, TRPS (top; ced-11) and TRPM (bottom; gon-2, gtl-1, and gtl-2) have nonoverlapping coexpressed gene networks. (D) Top, different GO terms are associated with C. elegans TRPS and TRPM coexpression networks. Bottom, only a single GO term, “cell surface receptor signaling pathway” (GO: 0007166), showed statistically significant enrichment in the TRPS gene network. This term does not appear for the TRPM network. GO terms are detailed in supplementary data S2 and S3, Supplementary Material online.
	Fig. 4. Summary of the evolution of TRPS channels. The TRPS family is largely restricted to protostome lineages. Figure derived from reconciled maximum likelihood tree of TRPS sequences (supplementary fig. S5, Supplementary Material online). Red dots and colored branches indicate phylum-specific duplication events. Gray and dashed branches indicate that no TRPS sequences were found for the indicated phylum and were inferred to be loss events.
	Fig. 5. Summary of the evolution of TRPM channels. The TRPM family is widely conserved and is present in all phyla surveyed except Tardigrada. Figure derived from consensus topologies in reconciled maximum likelihood trees generated against TRPM database sequences, with branch support for duplication branches extracted from phylograms without Xenacoelomorpha (supplementary figs. S13–S17, Supplementary Material online). Asterisk (*) indicates that a duplication branch most frequently formed due to rearrangement (initial UFboot branch support <95). Here, phyla were expanded/collapsed to more easily show TRPM diversification: Chordata was expanded into Cephalochordata (lancelets), Tunicata, and Vertebrata; Echinodermata and Hemichordata were collapsed into Ambulacraria; and Annelida, Nemertea, Brachiopoda, Phoronida, and Mollusca were collapsed into Lophotrochozoa. Red dots indicate duplication events. Dashed lines in color indicate sequences considered incertae sedis. Dashed lines in gray indicate that no sequences were found for the indicated taxon and were inferred to be loss events.
	Fig. 6. TRPM1-8 diversified soon after the vertebrate–tunicate split, and there is no evidence for TRPM8 in jawless, cartilaginous, or ray-finned fish. Figure derived from reconciled tree of chordate TRPM sequences (supplementary fig. S18, Supplementary Material online; see supplementary fig. S14, Supplementary Material online, for more visually accessible phylogram, which lacks ray-finned fish). An “X” indicates inferred gene loss, or lack of evidence of that gene in the indicated taxon.

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