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Evolution of Cilia Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Evolution of Cilia David R. Mitchell Department of Cell and Developmental Biology, SUNY Upstate Medical University, Syracuse, New York13210 Correspondence: [email protected] Anton van Leeuwenhoek’s startling microscopic observations in the 1600s first stimulated fascination with the way that cells use cilia to generate currents and to swim in a fluid environment. Research in recent decades has yielded deep knowledge about the mechanical and biochemical nature of these organelles but only opened a greater fascination about how such beautifully intricate and multifunctional structures arose during evolution. Answers to this evolutionary puzzle are not only sought to satisfy basic curiosity, but also, as stated so eloquently by Dobzhansky (Am Zool 4: 443 [1964]), because “nothing in biology makes sense except in the light of evolution.” Here I attempt to summarize current knowl- edge of what ciliary organelles of the last eukaryotic common ancestor (LECA) were like, explore the ways in which cilia have evolved since that time, and speculate on the selective processes that might have generated these organelles during early eukaryotic evolution. everal excellent papers have appeared in the and motility regulation, and these organisms Srecent past that follow evolution of structures include representatives of phylogenetically dis- or complexes essential to ciliary function, in- tant groups (green algae, ciliates, excavates, met- cluding reviews on basal bodies and centrioles azoa). Together with genomic data, these func- (Hodges et al. 2010; Ross and Normark 2015) tional and structural studies provide a basis and centrosomes (Azimzadeh 2014), trafficking for understanding common features of cilia and signaling modules (Johnson and Leroux that would have been present in the last com- 2010; Lim et al. 2011; Sung and Leroux 2013; mon ancestor as well as changes that may have Malicki and Avidor-Reiss 2014), tubulins (Fin- occurred since that time. These aspects of ciliary deisen et al. 2014), transition-zone complexes evolution can, therefore, be presented with only (Barker et al. 2014), and cilia themselves a modest level of speculation, and speculative (Satir et al. 2008; Carvalho-Santos et al. 2011). aspects are likely to be short-lived as additional Rather than attempting to cover all of the same data is collected. ground in a single review, I will refer the reader Knowing how cilia evolved in the first place, to other sources where appropriate and in- during those dark ages of eukaryotic evolu- stead try to look at the bigger pictures that are tion after formation of true eukaryotes but be- emerging from these details. Importantly, many fore diversification into currently recognized model organisms have contributed to studies supergroups, provides greater challenges. Evo- of cilia-related processes such as intraflagellar lutionary change includes continuous (as well transport (IFT) trafficking, centriole assembly, as sudden and catastrophic) extinctions, which Editors: Wallace Marshall and Renata Basto Additional Perspectives on Cilia available at www.cshperspectives.org Copyright # 2017 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a028290 Cite this article as Cold Spring Harb Perspect Biol 2017;9:a028290 1 Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press D.R. Mitchell for the most part leave no trace in the genomic distant branches of the tree of life. Such is cer- record of extant organisms. For larger, multicel- tainly the case with prokaryotes, whose division lular species and for those with hard shells or into eubacteria and archaea was largely depen- tests, fossils may provide some clues to morpho- dent on sequence comparisons, not shape, but logic features of extinct clades. For single-celled similar discoveries have been made among eu- eukaryotes that existed before the last eukaryot- karyotes such as oomycetes, which look like ic common ancestor (LECA), and especially for fungi but clearly belong in stramenopiles, and evidence of their motile mechanisms, fossils more recently with apusozoa, which resemble provide little information. We are, therefore, re- amoebae but are more closely related to us duced to analysis of genomic changes between (Paps et al. 2013; Cavalier-Smith et al. 2014). the closest living prokaryotic relatives of eu- The tree in Figure 1 summarizes many recent karyotes, as a proxy for the first eukaryotic an- studies on the relationships among extant eu- cestor, and the inferred common set of genes of karyotes. Disagreement remains on some of the LECA, to learn how cilia evolved. Missing the deep connections in this tree, in part because from this equation are data on other evolution- we still lack genomic sequences of some well- ary paths leading to development of motile or- known eukaryotes and in part because some ganelles (perhaps resembling cilia or perhaps genomes appear to be evolving so fast that rela- not) that might have flourished for some time tionships are difficult to establish. Of course but that became extinct and left no trace in the many other species remain to be discovered current record. and some of these could reveal previously un- appreciated relationships, but such trees remain useful because structures, mechanisms, and in- THE CILIATED ORGANELLE OF THE LECA dividual proteins that are found in multiple When it comes to single-celled organisms, there branches must have existed in the last common is only so much to be learned from morpho- ancestor of those divergent species, regardless of logical features. Many species that were once their true phylogenetic relationships. thought to be closely related, based on outward Comparison of many recently generated appearance, have turned out to belong to quite trees of eukaryotic phylogeny leads to two strik- 96-nm repeat A Bikonts B Dimeric ODAs Unikonts Excavata SAR Higher plants MIA complex Amoebozoa Green algae Dimeric IDA Metazoa Red algae Fungi Glaucophytes Base Tip Apusozoa Monomeric IDAs Spokes S1 S2 S3 Plastid DRC/nexin LECA Central pair complex Figure 1. (A) Diagram of major eukaryotic clades diverging from a last eukaryotic common ancestor (LECA), with the root placed between unikont and bikont superclades. Branches are color-coded according to differences in orientation of ciliary central-pair microtubules, which appear perpendicular to the bend plane and fixed in unikonts (blue), perpendicular to the bend plane but floating in excavates (orange), and twisted (helical) and rotating in other bikonts (green). The LECA is cartooned as a single cell with a nucleus, a mitochondrion, and two flagella: an anterior motile flagellum and a posterior gliding flagellum. The dashed arrow indicates the first acquisition of a plastid through endosymbiosis of a cyanobacterium. (B) Diagrams of ciliary axonemal struc- tures that were present in the LECA. (Left) Cross-sectional view from inside the cell. (Right) Longitudinal view of one 96-nm repeat along an outer doublet. MIA, Modifier of inner arms; ODA, outer dynein arm; IDA, inner dynein arm; DRC, dynein regulatory complex. 2 Cite this article as Cold Spring Harb Perspect Biol 2017;9:a028290 Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Evolution of Cilia ing conclusions. First, it is very difficult to sort singlet microtubules, assembled on basal bodies out the branch order at the base of the tree, built from nine triplet microtubules. Motility because all the major branches of eukaryotes generated by both outer and inner rows of dy- seem to have diverged from a common ancestor nein arms was regulated by interactions between within a short time (Fig. 1A). As with evolution radial spokes and a central-pair complex, and anywhere, anytime, branching is a continuous by nexin/dynein regulatory complex (DRC) in- process matched only by the frequency of ex- terdoublet links (Fig. 1B). Ciliary assembly tinction, so trees need to be interpreted by imag- required trafficking on IFT complexes, the re- ining what has been lost as well as what remains sulting organelles possessed sensory capabilities (Jablonski 1986). The effects of horizontal gene maintained in part by Bardet–Beidl syndrome transfer can sometimes make trees look more (BBS) complex-dependent receptor traffick- like webs (Soucy et al. 2015), but most existing ing, and movement of transmembrane proteins eukaryotes fit into one of several major clades could be used for transport of material along the related primarily by their decent from a com- ciliary surface or gliding motility of the cell. In mon ancestor. These include the Stramenopiles, short, these cilia would have been structurally Alveolates, Rhizaria (SAR); the Plantae (proba- and functionally indistinguishable from typical bly a sister group to the SAR); the excavates cilia seen today. (Heterolobosea, Euglenozoa, Diplomonads), which may be more closely related to the SAR TUBULINS, DOUBLETS, AND TRIPLETS than to the Plantae; the Amoebozoa; and the opisthokonts (Fungi, Choanozoa, Metazoa), Phylogenomics showsthat this ciliated LECAex- which are more closely related to Amoebozoa pressed a-, b-, g-, d-, 1-, and z-tubulin (Dutcher than to the other clades. These branches appear 2003; Findeisen et al. 2014). a-, b-, and g-tubu- to have originated in an evolutionary big bang, lin areessentially universal in eukaryotes, where- probably about one billion years ago (Cherni- as d-,1-, andz-tubulins areonly found in species kova et al. 2011; Parfrey et al. 2011). Second, the with cilia. Although not all organisms with cilia last common ancestor of all of these branches retain all three of these more divergent tubulin was highly complex (Koumandou et al. 2013). isoforms, they occur in diverse taxa, supporting It had to have everything that is now found, in their presence in the LECA (see Azimzadeh at least some representatives, in every branch. 2014 and Turk et al. 2015 for other recent over- Based on features common to eukaryotes in all views of centrioles and tubulin diversity).
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