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. 2022 Apr 25:10:867374.
doi: 10.3389/fcell.2022.867374. eCollection 2022.

The Amazing Evolutionary Complexity of Eukaryotic Tubulins: Lessons from Naegleria and the Multi-tubulin Hypothesis

Chandler Fulton  1
Affiliations

The Amazing Evolutionary Complexity of Eukaryotic Tubulins: Lessons from Naegleria and the Multi-tubulin Hypothesis

Chandler Fulton. Front Cell Dev Biol. .

Abstract

The multi-tubulin hypothesis proposed in 1976 was motivated by finding that the tubulin to build the flagellar apparatus was synthesized de novo during the optional differentiation of Naegleria from walking amoebae to swimming flagellates. In the next decade, with the tools of cloning and sequencing, we were able to establish that the rate of flagellar tubulin synthesis in Naegleria is determined by the abundance of flagellar α- and β-tubulin mRNAs. These experiments also established that the tubulins for Naegleria mitosis were encoded by separate, divergent genes, candidates for which remain incompletely characterized. Meanwhile an unanticipated abundance of tubulin isotypes has been discovered by other researchers. Together with the surprises of genome complexity, these tubulin isotypes require us to rethink how we might utilize the opportunities and challenges offered by the evolutionary diversity of eukaryotes.

Keywords: evolution; heterolobosea; microtubules; multi-tubulin; naegleria; protists; tubulin isotypes.

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Conflict of interest statement

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
The tubulin repertoire of Naegleria gruberi NEG. Interphase amoebae lack any cytoplasmic (or nuclear) microtubules. Dividing amoebae assemble mitotic tubulins (shown in orange) during their intranuclear mitosis. During the optional differentiation from amoebae to flagellates, induced by transfer from growth environment to nutrient-free buffer, the cells undergo a dramatic phenotypic change to rapidly swimming flagellates. The cells lose their capacity for amoeboid movement and round up. Basal bodies form and move to the cell surface, where they nucleate the growth of flagella. As the flagella elongate so do the cells, forming a streamlined shape with a cytoplasmic cytoskeleton of microtubules (shown in green). The differentiation can be made synchronous and temporarily reproducible. The graph shows the one-step differentiation experiment, measured as a quantal change (the appearance of flagella on fixed cell samples), and quantitative changes in flagellar tubulin mRNA and protein. See text for references.
FIGURE 2
FIGURE 2
The last eukaryotic common ancestor (LECA) of Naegleria and Chlamydomonas separated about 2,000 million years ago (Hedges et al., 2004), by which time LECA used microtubules for eukaryotic mitosis and for 9 + 2 flagellar axonemes with 9-triplet basal bodies. In Chlamydomonas, a single α-tubulin and single β-tubulin suffice for the mitotic spindle, the basal bodies, the flagella, and various accessory cytoplasmic microtubules in both dividing and swimming cells. In Naegleria, the flagellates synthesize very conserved α- and β-tubulin subunits to build the flagellar apparatus (shown in green), and some highly divergent protein(s) to assemble the mitotic spindle (shown in orange). The Chlamydomonas schematic diagrams are based on (Cross and Umen, 2015).
See this image and copyright information in PMC

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