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The World of Protozoa, Rotifera, Nematoda and Oligochaeta

[ref. ID; 7295 (O'Kelly, 1993)]

General morphology

Jakobid flagellates are minute, dorsiventrally organized, biflagellate, free-living, bacterivorous heterotrophs. The two flagella are anteriorly inserted and (sub)equal in length, with a hairpoint terminating at least the anterior flagellum. The posterior flagellum, which is the elder of the two, is recurrent, appressed to the ventral side of the cell but not fused with it. A cytoplasmic flap (the "lip") runs the length of the right ventral side of the cell, and the posterior flagellum lies in the groove thus formed. Bacteria are ingested in this region, but there is no cytostome. A single vane extends toward the cell body along most of the posterior flagellum's length. Neither the cell nor flagellar surface bears scales or hairs. Longitudinal cell division yields two progeny cells, at least one of which is an actively swimming naked planont with a reduced or absent right ventral lip and no vane on the posterior flagellum.

Relationships of the Jakobids

Jakobid genera are sister taxa

The ultrastructural features of interphase and dividing cells of these four heterotrophic flagellate genera, especially the cytoskeletal features, indicate to me that these taxa are more closely related to each other than to any other known group of mitochondrial protists. Flavin & Nerad (1993) and Patterson (1990) placed the genera they studied in Protista incertae sedis. Flavin & Nerad (1993) rejected the earlier proposal that Histiona is a bicosoecid (Mylnikov 1989).

Jakobid and retortamonads

Several structural features, in particular those of the cytoskeleton, link the jakobids to the metamonads in general and to the retortamonads in particular. Basal bodies in jakobids and metamonads are similar in length, internal structure, and in the features of the transition region, and the microtubular bands associated with the basal bodies are segregated into a dorsal fan and two ventral roots (Brugerolle 1991, 1993). Retortamonad cytoskeletal microtubules are associated with the cell periphery as in jakobids, while the peltas, axostyles, and nucleus-associated bands of diplomonads and oxymonads are absent. There is a remarkable similarity in basal body absolute configuration between the replicated flagellar apparatus of jakobids and the interphase flagellar apparatus of retotramonads, Chilomastix in particular. Cytoplasmic vanes on the recurrent flagellum of retortamonads are very similar in structure to those of jakobids. They are not found elsewhere among the metamonads except in the diplomonad Giardia, and diplomonads and retortamonads are arguably sister taxa (Brugerolle 1991). Spindle pole architecture is retortamonads and jakobids is very similar. Brugerolle (1977, 1991, 1990) considers the retortamonad spindle to be closed, but the few available pictures (Brugerolle 1973, 1977) do not rule out the possibility that the nuclear membrane is present during prophase but absent by metaphase as in the jakobids. The organization of the jakobid spindle into two half-spindles with no interzonal spindle apparent is consistent with light microscope interpretations of spindle architecture in retortamonads (Brugerolle 1973, 1993; Brugerolle and Migot 1990). Finally, the existence of free-living retortamonads (Brugerolle 1991, 1993; Brugerolle and Mignot 1990; Farmer 1993; Larsen and Patterson 1990 as Percolomonas cuspidata Larsen and Patterson 1990), indicates that the features of commensal retortamonads flagellates need not be derived in response to the commensal habitat.

Jakobids are not retortamonads

In addition to mitochondria, jakobids have differentiated Golgi bodies. Jakobid trophic cells lack cytostomes, rhizoplast-like organelles connecting the basal bodies to the nucleus, and complex structural elements in the distal portions of the ventral microtubular roots. Jakobid cysts have relatively thin walls with plugs, and do not contain flagellar axonemes. I regard jakobids and retortamonads as sister taxa.

The significance of the mitochondria

Elsewhere among the protists, organisms that share nucleocytoplasmic features to the same degree as do the jakobids have mitochondria with similar structure. Mitochondrial cristal structure therefore is one of the principal diagnostic features used in contemporary protist classifications (Corliss 1984; Page and Blanton 1985; Patterson 1988; Patterson and Brugerolle 1988). But among the jakobids, all the major mitochondrial structural types are found: flattened cristae in Jakoba, tubular cristae in Histiona and Reclinomonas, discoidal cristae in the undescribed species. Does this finding mean that mitochondrial cristae structure is untrustworthy as an indicator of phylogenetic relationships among protists? I think not. The feature is too consistent in other protist lineages to dismiss. Rather, the diversity of mitochodrial structure in jakobids reinforces my impressions that jakobids are closely related to the first mitochondrial protist(s). It may be that mitochondria in the first eukaryotes are of polyphyletic ancestry, with the different structural types seen in the earliest mitochondrial protists representing independent capture events of different bacterial species closley related eukaryotes, more or less as proposed by Stewart & Mattox (1984). Or, perhaps mitochondria are of monophyletic origin, and the divergences in mitochondrial structure in the first descendants of the single mitochodrial protist ancestor occurred early in the evolution of the endosymbiosis, perhaps as a consequence of the supposed early and massive transfer of genes from endosymbiont to host (Gray 1992). Either sequence of events, occurring in retortamonads, would produce a group of organisms with features very like those of the jakobids.

Jakobids and other mitochondrial protists

Certain ultrastructural features in various mitochondrial protists, including those with discoidal, those with tubular, and those with flattened mitochondrial cristae, suggest that the most ancestral protists in each of these three groups has a close phylogenetic relationship with the jakobids. I have space here only to present some of the more significant similarities and inferences. Jakobids and heteroloboseans (discoidal mitochondrial cristae) share features of the basal body transition region and root architecture, in particular the presence of a dorsal root in the unnamed jakobid species and in Percolomonas (Fenchel and Patterson 1986). One heterolobosean flagellate, Psalterimonas lanterna (Broers et al. 1990), has a vane, similar to that of jakobids and retrotamonads, on the posterior flagella. Cavalier-Simith (1991) has treated the heteroloboseans ("Percolozoa") as the most ancestral mitochondrial eukaryotes. I suggests, rather, that heteroloboseans are derived with respect to jakobids with discoidal cristae. Jakobids also share some ultrastructural features with the heterotrophic flagellate Colponema (tubular mitochondrial cristae) (Mignot and Brugerolle 1975). Colponema cells have a vane on the posterior flagellum; to date no other mitochondrial protists except the jakobids, Psalteriomonas and Colponema are known to possess this structure. There is a dorsal microtubular band and two ventral microtubular roots in the flagellar apparatus, with the latter defining a ventral furrow/cytostome complex. There is some jakobid extrusomes. Cavalier-Smith (1991) has treated Colponema as a near-ancestral member of his Kingdom Alveolata (ciliates, dinoflagellates, apicomplexans). I suggest that Colponema is derived relative to jakobids with tubular mitochondrial cristae. Two structural features suggest to me that an evolutionary relationship exists between the jakobids and the green algae (flattened mitochondrial cristae), especially the phycomate prasinophytes, which I believe are the most ancestral green plants (O'Kelly 1992). The three-dimension architecture of the replicated basal body complex in jakobids has much in common with phycomate prasinophytes, Halosphaera in particular. Also, the multilayered structure (MLS) in Reclinomonas, as is its less well defined (degenerate?) couterpart in Jakoba, is attached to the eldest basal body and borne on the proximal end of a spline-type microtubular root corresponding to root "1d" (terminology of Moestrup and Hori 1989) in green plants. The presence of the MLS in jakobids with both flattened and tubular cristae may explain in part how MLS have come to be reported in several diverse lineages of eukaryotes (Wilcox 1989). Cavalier-Smith (1991) suggested a close phylogenetic link between jakobids and his Phylum Choanozoa, but there are certainly fewer ultrastructural similarities, especially in flagellar apparatus features, between jakobids and choanoflagellates than there are between jakobids and green alage.

The classification of jakobids

Jakobids are closely related on the basis of what we know of their nucleocytoplasmic features. Nevertheless it is no simple matter to determine a classification for them. If the jakobids are treated as a grade, then a single higher taxon may be established, for which the family name Jakobidae Patterson, 1990, is correct. If, however, the jakobids are treated as members of clades, and my interpretation of the clades involved proves, on further research, to be correct, then any taxon created on what I have called "jakobids" is paraphyletic and therefore inadmissible. Three higher taxa are necessary: Jakobidae, Histionidae Flavin & Nerad, and a third for the undescribed species. This difficulty is a microcosm of the problems facing the entire field of eukaryote classification, especially as it pertains to protists (Corliss 1990; Patterson and Larsen 1992; Patterson and Zolffel 1991). My view is that until the clades of protist evolution are between known, it is futile to attempt to convey grade information in a formal classification and expect such a classification to be uncontroversial and stable. Hence the increasing use of "common" names (jakobids, for example) to denote eukaryotes taxa whose phylogenetic relationships are under investigation.