Hatena arenicola gen. et sp. nov., a Katablepharid Undergoing Probable Plastid Acquisition

Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1, Tennodai, Tsukuba, Ibaraki 305-8572, Japan.
Protist (Impact Factor: 3.05). 11/2006; 157(4):401-19. DOI: 10.1016/j.protis.2006.05.011
Source: PubMed


Hatena arenicola gen. et sp. nov., an enigmatic flagellate of the katablepharids, is described. It shows ultrastructural affinities to the katablepharids, including large and small ejectisomes, cell covering, and a feeding apparatus. Although molecular phylogenies of the 18S ribosomal DNA support its classification into the katablepharids, the cell is characterized by a dorsiventrally compressed cell shape and a crawling motion, both of which are unusual within this group. The most distinctive feature of Hatena arenicola is that it harbors a Nephroselmis symbiont. This symbiosis is distinct from previously reported cases of ongoing symbiosis in that the symbiont plastid is selectively enlarged, while other structures such as the mitochondria, Golgi body, cytoskeleton, and endomembrane system are degraded; the host and symbiont have developed a morphological association, i.e., the eyespot of the symbiont is always at the cell apex of Hatena arenicola; and only one daughter cell inherits the symbiont during cell division, resulting in a symbiont-bearing green cell and a symbiont-lacking colorless cell. Interestingly, the colorless cells have a feeding apparatus that corresponds to the location of the eyespot in symbiont-bearing cells, and they are able to feed on prey cells. This indicates that the morphology of the host depends on the presence or absence of the symbiont. These observations suggest that Hatena arenicola has a unique "half-plant, half-predator" life cycle; one cell divides into an autotrophic cell possessing a symbiotic Nephroselmis species, and a symbiont-lacking colorless cell, which later develops a feeding apparatus de novo. The evolutionary implications of Hatena arenicola as an intermediate step in plastid acquisition are discussed in the context of other examples of ongoing endosymbioses in dinoflagellates.

Download full-text


Available from: Noriko Okamoto, Oct 04, 2015
179 Reads
  • Source
    • "For example , the marine katablepharid protist Hatena arenicola harboring the green alga Nephroselmis sp. (Okamoto and Inouye 2006) and the freshwater euglenid Petalomonas sphagnophila associating with several different kinds of endosymbiotic bacteria (Kim et al. 2010), have not been cultured despite numerous efforts. Furthermore, the symbiotic relationships could be altered during the culturing procedures, such as elimination of one or more partners in the case of facultative associations (e.g. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The discovery and characterization of protist communities from diverse environments are crucial for understanding the overall evolutionary history of life on earth. However, major questions about the diversity, ecology, and evolutionary history of protists remain unanswered, notably because data obtained from natural protist communities, especially of heterotrophic species, remain limited. In this review, we discuss the challenges associated with "field protistology", defined here as the exploration, characterization, and interpretation of microbial eukaryotic diversity within the context of natural environments or field experiments, and provide suggestions to help fill this important gap in knowledge. We also argue that increased efforts in field studies that combine molecular and microscopical methods offer the most promising path toward (1) the discovery of new lineages that expand the tree of eukaryotes; (2) the recognition of novel evolutionary patterns and processes; (3) the untangling of ecological interactions and functions, and their roles in larger ecosystem processes; and (4) the evaluation of protist adaptations to a changing climate. This article is protected by copyright. All rights reserved.
    Journal of Eukaryotic Microbiology 12/2013; 61(2). DOI:10.1111/jeu.12095 · 3.22 Impact Factor
  • Source
    • "Based on size, morphology, and location with in the cells, three types (I, II, and III) are described for Leucocryptos marina (Vørs 1992). Two types, differentiated on the basis of size (types I and II), can be found in Kathablepharis species (Clay and Kugrens 1999a, b) and Hatena arenicola (Okamoto and Inouye 2006). The ejectisomes of the kathablepharid Roombia truncata are aligned in five to 11 rows showing a size gradient within each row: type II-sized ones, ca. "
    [Show abstract] [Hide abstract]
    ABSTRACT: For the first time, ejectisome-enriched fractions were isolated from the marine prasinophyte Pyramimonas grossii. Transmission electron microscopy revealed that most of the ejectisomes were discharged and formed long, spirally twisted filaments. Some ejectisomes were still fully or partly furled. Discharged ejectisomes measured up to 26 μm in length and 200 nm in width; those still furled measured up to 900 nm in width and 1,000 nm in length. Particle periodicities of approximately 4.2 and 5.8 nm could be measured from freeze-fractured filaments. Sodium dodecyl sulfate polyacrylamide gel electrophoresis revealed a protein banding pattern, dominated by polypeptides of 16-20 kDa. These polypeptides were not glycosylated and did not cross-react with antisera directed against recombinant R-body polypeptides of Caedibacter taeniospiralis or directed against reconstituted cryptophycean ejectisomes.
    Protoplasma 06/2013; 250(6). DOI:10.1007/s00709-013-0518-7 · 2.65 Impact Factor
  • Source
    • "Katablepharis spp., L. marina, and P. psammobia form swarms when they attack prey, attaching to small cells directly at the cell apex and then engulfing them [35], [41], or myzocytotically taking up the cytoplasm of larger prey (Okamoto, preliminary observations). In contrast, H. arenicola does not form a swarm, but engulfs a small prey cell without changing cell shape [10]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Photosynthetic eukaryotes with a secondary plastid of red algal origin (cryptophytes, haptophytes, stramenopiles, dinoflagellates, and apicomplexans) are hypothesized to share a single origin of plastid acquisition according to Chromalveolate hypothesis. Recent phylogenomic analyses suggest that photosynthetic "chromalveolates" form a large clade with inclusion of several non-photosynthetic protist lineages. Katablepharids are one such non-photosynthetic lineage closely related to cryptophytes. Despite their evolutionary and ecological importance, katablepharids are poorly investigated. Here, we report a newly discovered flagellate, Roombia truncata gen. et sp. nov., that is related to katablepharids, but is morphologically distinct from othermembers of the group in the following ways: (1) two flagella emerge from a papilla-like subapical protrusion, (2) conspicuous ejectisomes are aligned in multiple (5-11) rows, (3) each ejectisome increases in size towards the posterior end of the rows, and (4) upon feeding, a part of cytoplasm elastically stretch to engulf whole prey cell. Molecular phylogenies inferred from Hsp90, SSU rDNA, and LSU rDNA sequences consistently and strongly show R. truncata as the sister lineage to all other katablepharids, including lineages known only from environmental sequence surveys. A close association between katablepharids and cryptophytes was also recovered in most analyses. Katablepharids and cryptophytes are together part of a larger, more inclusive, group that also contains haptophytes, telonemids, centrohelids and perhaps biliphytes. The monophyly of this group is supported by several different molecular phylogenetic datasets and one shared lateral gene transfer; therefore, we formally establish this diverse clade as the "Hacrobia." Our discovery of R. truncata not only expands our knowledge in the less studied flagellate group, but provide a better understanding of phylogenetic relationship and evolutionary view of plastid acquisition/losses of Hacrobia. Being an ancestral to all katablepharids, and readily cultivable, R. truncata is a good candidate for multiple gene analyses that will contribute to future phylogenetic studies of Hacrobia.
    PLoS ONE 09/2009; 4(9):e7080. DOI:10.1371/journal.pone.0007080 · 3.23 Impact Factor
Show more