TIAMMAt: leveraging biodiversity to revise protein domain models, evidence from innate immunity

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Tassia, M. G., David, K. T., Townsend, J. P., & Halanych, K. M. TIAMMAt: leveraging biodiversity to revise protein domain models, evidence from innate immunity. Molecular Biology and Evolution, 38(12), (2021): 5806–5818, https://doi.org/10.1093/molbev/msab258.Sequence annotation is fundamental for studying the evolution of protein families, particularly when working with nonmodel species. Given the rapid, ever-increasing number of species receiving high-quality genome sequencing, accurate domain modeling that is representative of species diversity is crucial for understanding protein family sequence evolution and their inferred function(s). Here, we describe a bioinformatic tool called Taxon-Informed Adjustment of Markov Model Attributes (TIAMMAt) which revises domain profile hidden Markov models (HMMs) by incorporating homologous domain sequences from underrepresented and nonmodel species. Using innate immunity pathways as a case study, we show that revising profile HMM parameters to directly account for variation in homologs among underrepresented species provides valuable insight into the evolution of protein families. Following adjustment by TIAMMAt, domain profile HMMs exhibit changes in their per-site amino acid state emission probabilities and insertion/deletion probabilities while maintaining the overall structure of the consensus sequence. Our results show that domain revision can heavily impact evolutionary interpretations for some families (i.e., NLR’s NACHT domain), whereas impact on other domains (e.g., rel homology domain and interferon regulatory factor domains) is minimal due to high levels of sequence conservation across the sampled phylogenetic depth (i.e., Metazoa). Importantly, TIAMMAt revises target domain models to reflect homologous sequence variation using the taxonomic distribution under consideration by the user. TIAMMAt’s flexibility to revise any subset of the Pfam database using a user-defined taxonomic pool will make it a valuable tool for future protein evolution studies, particularly when incorporating (or focusing) on nonmodel species.This work was supported by The National Science Foundation (Grant No. IOS—1755377 to K.M.H., Rita Graze, and Elizabeth Hiltbold Schwartz), and K.T.D. was supported by The National Science Foundation’s Graduate Research Fellowship Program

Benthic Macrofauna Abundance Along a Transect from False Bay, San Juan Island

Benthic macrofauna are a diverse group of organisms found in both deep-sea and shallow-water systems. Understanding the influence of biotic and abiotic factors in shallow-water systems can translate to further understanding inaccessible deep-sea community structure. This study observes the change in community structure as a function of ‘Altitude Above Mean Low-tide Sea-level’ (AAML) and distance from shore through push-core sediment sampling. In addition, this study identifies several specimens through genetic barcoding methods. The results show closer relationship among 90cm AAML sites than between any 90cm and 60cm site. Finally, specimens identified through barcoding could not be identified down to a species level. Future population genetic analyses will benefit from increasing accessibility to metagenetics and high-throughput sequencing

Benthic Macrofauna Abundance Along a Transect from False Bay, San Juan Island

Benthic macrofauna are a diverse group of organisms found in both deep-sea and shallow-water systems. Understanding the influence of biotic and abiotic factors in shallow-water systems can translate to further understanding inaccessible deep-sea community structure. This study observes the change in community structure as a function of ‘Altitude Above Mean Low-tide Sea-level’ (AAML) and distance from shore through push-core sediment sampling. In addition, this study identifies several specimens through genetic barcoding methods. The results show closer relationship among 90cm AAML sites than between any 90cm and 60cm site. Finally, specimens identified through barcoding could not be identified down to a species level. Future population genetic analyses will benefit from increasing accessibility to metagenetics and high-throughput sequencing

Data from: Phylogenomics offers resolution of major tunicate relationships

Tunicata, a diverse clade of approximately 3,000 described species of marine, filter-feeding chordates, is of great interest to researchers because tunicates are the closest living relatives of vertebrates and they facilitate comparative studies of our own biology. The group also includes numerous invasive species that cause considerable economic damage and some species of tunicates are edible. Despite their diversity and importance, relationships among major lineages of Tunicata are not completely resolved. Here, we supplemented public data with transcriptomes from seven species spanning the diversity of Tunicata and conducted phylogenomic analyses on data sets of up to 798 genes. Sensitivity analyses were employed to examine the influences of reducing compositional heterogeneity and branch-length heterogeneity. All analyses maximally supported a monophyletic Tunicata within Olfactores (Vertebrata + Tunicata). Within Tunicata, all analyses recovered Appendicularia sister to the rest of Tunicata and confirmed (with maximal support) that Thaliacea is nested within Ascidiacea. Stolidobranchia is the sister taxon to all other tunicates except Appendicularia. In most analyses, phlebobranch tunicates were recovered paraphyletic with respect to Aplousobranchia. Support for this topology varied but was strong in some cases. However, when only the 50 best genes based on compositional heterogeneity were analysed, we recovered Phlebobranchia and Aplousobranchia reciprocally monophyletic with strong support, consistent with most traditional morphology-based hypotheses. Examination of internode certainty also cast doubt on results of phlebobranch paraphyly, which may be due to limited taxon sampling. Taken together, these results provide a higher-level phylogenetic framework for our closest living invertebrate relatives

Biogeographical Distribution of Enteropneust and Pterobranch species.

<p>Depiction of the number of unique species reported in each geographic region. Geographic regions are adapted from the marine provinces of Spalding et al. 2007 [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref088" target="_blank">88</a>]. These numbers are an underestimation of true species diversity, as there are manuscripts <i>in preparation</i> and many described specimens [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref033" target="_blank">33</a>]. See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.s001" target="_blank">S1 Table</a> for detailed marine province information. Map image: Courtesy of VLIMAR [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref102" target="_blank">102</a>]. Figure modified from source material in reference [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref088" target="_blank">88</a>]. Original figure: <a href="http://www.marineregions.org/gazetteer.php?p=image&pic=64936" target="_blank">http://www.marineregions.org/gazetteer.php?p=image&pic=64936</a>.</p

Deuterostome Phylogeny.

<p>Consensus relationships among deuterostome taxa are shown. Current data provides high-support for Classes Pterobranchia and Enteropneusta as reciprocally monophyletic. In addition, phylogenomic evidence suggests the enteropneust family, Torquaratoridae, fall within the Ptychoderidae. This tree utilizes consolidated data from 16S +18S rRNA, and phylogenomic studies from multiple sources [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref015" target="_blank">15</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref027" target="_blank">27</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref028" target="_blank">28</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref100" target="_blank">100</a>].</p

Images of Hemichordate Species found around the World.

<p>A) <i>Ptychodera flava</i> (the Hawaiian acorn worm), has been found in many different marine ecoregions of the world. It was the first described hemichordate species [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref002" target="_blank">2</a>]. B) <i>Saccoglossus bromophenolosus</i> has been found in the waters of Maine and Washington state. This species was apparently introduced from Maine to Washington due to the oyster industry in the early 1900s [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref045" target="_blank">45</a>]. C) Zooid of the pterobranch <i>Cephalodiscus gracilis</i>, a species found in Bermuda. D) <i>Rhabdopleura normani</i> zooids living within a coenecium. Images: A) and B) photo credit Billie J. Swalla, C) and D) photo credit Kenneth M. Halanych.</p

A Timeline of Hemichordate Species Discovery.

<p>A) The cumulative number of new enteropneust and pterobranch species descriptions per year is shown. B) The percentage of species described according to author. For example, ‘single-species authors’ indicates 37% of species were described by authors whom described only a single hemichordate in his/her career. Reports by Ritter alone (4) are not binned with Cameron et al. descriptions (e.g. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref101" target="_blank">101</a>] and [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref077" target="_blank">77</a>], respectively). Only extant species are included.</p

Body Plans of Hemichordate Species present Throughout the World.

<p>Commonly studied free-living acorn worms (enteropneusts) include members of the A) Ptychoderidae and B) Harrimaniidae. Enteropneusts have most often been found in coastal areas in shallow and deep waters. In contrast, extant pterobranchs C) Cephalodiscidae and D) Rhabdopleuridae often inhabit the deep sea and southern polar regions, but some also occur in warm shallow water. Pterobranch species are colonial and individuals are connected to each other via long, branched stalks. Redrawn from Rychel and Swalla (2009) [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0162564#pone.0162564.ref065" target="_blank">65</a>].</p