The term “karyomastigont” was coined by Janicki (23) to refer to a conspicuous organellar system he observed in certain protists: the mastigont (“cell whip,” eukaryotic flagellum, or undulipodium, the [9 (2) + (2)] microtubular axoneme underlain by its [9 (3) + 0)] kinetosome) attached by a “nuclear connector” or “rhizoplast” to a nucleus. The need for a term came from Janicki's work on highly motile trichomonad symbionts in the intestines of termites where karyomastigonts dominate the cells. When kinetosomes, nuclear connector, and other components were present but the nucleus was absent from its predictable position, Janicki called the organelle system an “akaryomastigont.” In the Calonymphidae, one family of entirely multinucleate trichomonads, numerous karyomastigonts, and akaryomastigonts are simultaneously present in the same cell (e.g., Calonympha grassii) (24).
The karyomastigont, an ancestral feature of eukaryotes, is present in “early branching protists” (25–27). Archaeprotists, a large inclusive taxon (phylum of Kingdom Protoctista) (7) are heterotrophic unicells that inhabit anoxic environments. All lack mitochondria. At least 28 families are placed in the phylum Archaeprotista. Examples include archaemoebae (Pelomyxa and Mastigamoeba), metamonads (Retortamonas), diplomonads (Giardia), oxymonads (Pyrsonympha), and the two orders of Parabasalia: Trichomonadida [Devescovina, Mixotricha, Monocercomonas, Trichomonas, and calonymphids (Coronympha, Snyderella)] and Hypermastigida (Lophomonas, Staurojoenina, and Trichonympha). These cells either bear karyomastigonts or derive by differential organelle reproduction (simple morphological steps) from those that do (Table 1). When, during evolution of these protists, nuclei were severed from their karyomastigonts, akaryomastigonts were generated (31). Nuclei, unattached, at least temporarily, to undulipodia were freed to proliferate and occupy central positions in cells. Undulipodia, also freed to proliferate, generated larger, faster-swimming cells in the same evolutionary step.
The karyomastigont is the conspicuous central cytoskeleton in basal members of virtually all archaeprotist lineages [three classes: Archamoeba, Metamonads, and Parabasalia (32)] (Fig. 2). In trichomonads, the karyomastigont, which includes a parabasal body (Golgi complex), coordinates the placement of hydrogenosomes (membrane-bounded bacterial-sized cell inclusions that generate hydrogen). The karyomastigont reproduces as a unit structure. Typically, four attached kinetosomes with rolled sheets of microtubules (the axostyle and its extension the pelta) reproduce as their morphological relationships are retained. Kinetosomes reproduce first, the nucleus divides, and the two groups of kinetosomes separate at the poles of a thin microtubule spindle called the paradesmose. Kinetosomes and associated structures are partitioned to one of the two new karyomastigonts. The other produces components it lacks such as the Golgi complex and axostyle.
Nuclear α-proteobacterial genes were interpreted to have originated from lost or degenerate mitochondria in at least two archaeprotist species [Giardia lamblia (33); Trichomonas vaginalis (34, 35)] and in a microsporidian (36). Hydrogenosomes, at least some types, share common origin with mitochondria. In the hydrogen hypothesis (20), hydrogenosomes are claimed to be the source of eubacterial genes in amitochondriates. That mitochondria were never acquired in the ancestors we consider more likely than that they were lost in every species of these anaerobic protists. Eubacterial genes in the nucleus that are not from the original spirochete probably were acquired in amitochondriate protists from proteobacterial symbionts other than those of the mitochondrial lineage. Gram-negative bacteria, some of which may be related to ancestors of hydrogenosomes, are rampant as epibionts, endobionts, and even endonuclear symbionts—for example, in Caduceia versatilis (37).
Karyomastigonts freed (detached from) nuclei independently in many lineages both before and after the acquisition of mitochondria. Calonymphid ancestors of Snyderella released free nuclei before the mitochondrial symbiosis (13), and Chlamydomonas-like ancestors of other chlorophytes such as Acetabularia released the nuclei after the lineage was fully aerobic (38). In trophic forms of protists that lack mastigote stages, the karyomastigont is generally absent. An exception is Histomonas, an amoeboid trichomonad cell that lacks an axoneme but bears enough of the remnant karyomastigont structure to permit its classification with parabasalids rather than with rhizopod amoebae (39). This organellar system appears in the zoospores, motile trophic forms, or sperm of many organisms, suggesting the relative ease of karyomastigont development. The karyomastigont, apparently in some cells, is easily lost, suppressed, and regained. In many taxa of multinucleate or multicellular protists (foraminifera, green algae) and even in plants, the karyomastigont persists only in the zoospores or gametes.
In yeast, nematode, insect, and mammalian cells, nonkaryomastigont microtubule-organizing centers are “required to position nuclei at specific locations in the cytoplasm” (40). The link between the microtubule organizing center and the nuclei “is mysterious” (40). To us, the link is an evolutionary legacy, a remnant of the original archaebacterial-eubacterial connector. The modern organelles (i.e., centriole-kinetosomes, untethered nuclei, Golgi, and axostyles) derive from what first ensured genetic continuity of the chimera's components: the karyomastigont, a structure that would have been much more conspicuous to Proterozoic investigators than to us.