Ultrastructure of the sperm axoneme and molecular analysis of axonemal dynein in ephemeroptera (Insecta)

Abstract

The Ephemeroptera sperm axoneme is devoid of outer dynein arms (ODA) and exhibits a pronounced modification of the central pair complex (CPC), which is substituted by the central sheath (CS): a tubular element of unknown molecular composition. We performed a detailed ultrastructural analysis of sperm axonemes in the genera Cloeon and Ecdyonurus using quick-freeze, deep-etch electron microscopy, showing that the loss of the conventional CPC is not only concomitant with the loss of ODA, but also with a substantial modification in the longitudinal distribution of both radial spokes (RS) and inner dynein arms (IDA). Such structures are no longer distributed following the alternation of different repeats as in the 9 + 2 axoneme, but instead share a 32 nm longitudinal repeat: a multiple of the 8 nm repeat observed along the CS wall. Differently from the conventional CPC, the CS and the surrounding RS possess a ninefold symmetry, coherently with the three-dimensional pattern of motility observed in Cloeon free spermatozoa. Biochemical analyses revealed that ultrastructural modifications are concomitant with a reduced complexity of the IDA heavy chain complement. We propose that these structural and molecular modifications might be related to the relief from the evolutionary constraints imposed by the CPC on the basal 9 + 9 + 2 axoneme and could also represent the minimal set compatible with flagellar beating and progressive motility mechanically regulated as suggested by the geometric clutch hypothesis. © 2014 Wiley Periodicals, Inc.

Composition and function of ciliary inner‐dynein‐arm subunits studied in Chlamydomonas reinhardtii

“…Also, in cilia from Drosophila chordotonal neurons, IDAs f/I1 and g may not assemble, while other IDAs can assemble properly (Zur Lage, Newton, & Jarman, 2019). In addition, a recent report indicated that sperm cilia from two species of Ephemeroptera (mayfly), Ecdyonurus venosus and Cloeon dipterum lack ODAs and bear a unique arrangement of IDAs (Mencarelli, Mercati, Dallai, & Lupetti, 2014). These sperm cilia have an unusual “9 + 9 + 0” axonemal organization that contains accessory microtubules, but lacks a central pair complex (Mencarelli et al, 2014).…”

“…In addition, a recent report indicated that sperm cilia from two species of Ephemeroptera (mayfly), Ecdyonurus venosus and Cloeon dipterum lack ODAs and bear a unique arrangement of IDAs (Mencarelli, Mercati, Dallai, & Lupetti, 2014). These sperm cilia have an unusual “9 + 9 + 0” axonemal organization that contains accessory microtubules, but lacks a central pair complex (Mencarelli et al, 2014). Predictably, these cilia generate lower beat frequency compared to Chlamydomonas .…”

“…Moreover, these axonemes appear to contain one species of DHC suggesting Ephemeroptera has only one species of IDA. If this is true, then one type of IDA can drive progressive motility and rhythmic beating in these sperm axonemes (Mencarelli et al, 2014). It will be important to identify the IDA DHCs in Chlamydomonas and vertebrates that is homologous to the insect dynein.…”

The geometric clutch at 20: stripping gears or gaining traction?

“…These strange flagella are often still capable of rhythmic beating and flagellar propulsion. The latest example of this is presented in a beautiful study by Mencarelli et al (2014) for mayfly sperm. These sperm seem to retain only one type of inner-arm dynein and are missing most of the components of the cp-spoke apparatus.…”

The evolution of sperm axoneme structure and the dynein heavy chain complement in cecidomid insects

“…Mutant Chlamydomonas strains with large defects in the inner dynein arms are immotile [Kurimoto and Kamiya, ]. Moreover, while axonemes endowed with only the inner dynein arms are expressed in diverse organisms [Gibbons et al, ; Hyams and Campbell, ; Dallai et al, ; Dallai and Afzelius, ; Woolley, ; Lupetti et al, ; Dallai, ; Mencarelli et al, ;] and are still motile, an extremely limited number of protozoan and metazoan species are known which express axonemes whose motility is based only on the activity of outer dynein arms [Dallai, ; Dallai et al, ; Wickstead and Gull, ; Mencarelli et al, ]. Interestingly, all the metazoan species are comprised in the same group of insects, the dipteran family Cecidomyiidae [Dallai, ; Dallai et al, ; Mencarelli et al, ].…”