Taxon-specific expansion and loss of tektins inform metazoan ciliary diversity

Benjamin R Bastin,Stephan Q Schneider

doi:10.1186/s12862-019-1360-0

Abstract

BackgroundCilia and flagella are complex cellular structures thought to have first evolved in a last ciliated eukaryotic ancestor due to the conserved 9 + 2 microtubule doublet structure of the axoneme and associated proteins. The Tektin family of coiled-coil domain containing proteins was previously identified in cilia of organisms as diverse as green algae and sea urchin. While studies have shown that some Tektins are necessary for ciliary function, there has been no comprehensive phylogenetic survey of tektin genes. To fill this gap, we sampled tektin sequences broadly among metazoan and unicellular lineages in order to determine how the tektin gene complements evolved in over 100 different extant species.ResultsUsing Bayesian and Maximum Likelihood analyses, we have ascertained with high confidence that all metazoan tektins arose from a single ancestral tektin gene in the last common ancestor of metazoans and choanoflagellates. Gene duplications gave rise to two tektin genes in the metazoan ancestor, and a subsequent expansion to three and four tektin genes in early bilaterian ancestors. While all four tektin genes remained highly conserved in most deuterostome and spiralian species surveyed, most tektin genes in ecdysozoans are highly derived with extensive gene loss in several lineages including nematodes and some crustaceans. In addition, while tektin-1, − 2, and − 4 have remained as single copy genes in most lineages, tektin-3/5 has been duplicated independently several times, notably at the base of the spiralian, vertebrate and hymenopteran (Ecdysozoa) clades.ConclusionsWe provide a solid description of tektin evolution supporting one, two, three, and four ancestral tektin genes in a holozoan, metazoan, bilaterian, and nephrozoan ancestor, respectively. The isolated presence of tektin in a cryptophyte and a chlorophyte branch invokes events of horizontal gene transfer, and that the last common ciliated eukaryotic ancestor lacked a tektin gene. Reconstructing the evolutionary history of the tektin complement in each extant metazoan species enabled us to pinpoint lineage specific expansions and losses. Our analysis will help to direct future studies on Tektin function, and how gain and loss of tektin genes might have contributed to the evolution of various types of cilia and flagella.

Highlights

Cilia and flagella are complex cellular structures thought to have first evolved in a last ciliated eukaryotic ancestor due to the conserved 9 + 2 microtubule doublet structure of the axoneme and associated proteins
Number of metazoan tektin genes in eukaryotic genomes To elucidate the evolutionary history of the tektin gene family, we used reciprocal BLAST searches to survey 109 species from the major metazoan lineages with a preference for phylogenetically informative taxa along with 17 unicellular species (Additional file 1)
At least one tektin sequence was identified in 111 different species including all representatives from all major metazoan phyla except Placozoa as well as two choanoflagellates and four other unicellular organisms from the Chlorophyta and Cryptophyta

Summary

Introduction

Cilia and flagella are complex cellular structures thought to have first evolved in a last ciliated eukaryotic ancestor due to the conserved 9 + 2 microtubule doublet structure of the axoneme and associated proteins. The presence of motile cilia and flagella as a means of providing motility in unicellular organisms such as the paramecium and the green algae Chlamydomonas reinhardtii indicate an ancient conserved role for these structures in providing cellular motility [1, 4] This role is conserved in a variety of metazoan species as well, both in embryonic and adult stages. In sponges a specialized cell type utilizes the beating of flagella to create fluid flow and actively pump water for filtration, removing food particles for phagocytosis This cell type has been named ‘choanocytes’ due to their similarity in form and function to choanoflagellates, the group of unicellular organisms that is considered sister group to metazoans [17]

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