Two parasitic ciliates (Protozoa: Ciliophora: Phyllopharyngea) isolated from respiratory-mucus of an unhealthy beluga whale: characterization, phylogeny and an assessment of morphological adaptations

Abstract

Ciliates occur in the blowholes of marine mammals, but our understanding of their biology is poor. Consequently, we investigated an infestation of ciliates in an unhealthy, captive beluga whale that was exhibiting accelerated breathing, leukocytosis and expulsion of unusually large amounts of viscous sputum. This sputum contained ~104 ciliates mL-1 (when healthy, numbers were ten- to 100-fold lower). One known ciliate species, Planilamina ovata, is fully characterized, and a new species, Kyaroikeus paracetarius sp. nov., is here described. The new species is established based on its larger number of left kineties over its only congener. Sequences of small-subunit rDNA, large-subunit rDNA and ITS1-5.8S-ITS2 regions of these two taxa were used in phylogenetic analyses, inferring that Kyaroikeus and Planilamina have close affinity with the free-living family Dysteriidae, contradicting their morphology-based assignment to the family Kyaroikeidae. We suggest that Kyaroikeidae be relegated to subfamily status. Finally, by comparing parasitic species with free-living taxa, we suggest how these ciliates have adapted to their unique environment and how they may have initially invaded the host. We provide essential data and concepts for the continued evaluation of ciliate-parasites in whale blowholes.

Historical Review of Studies on Cyrtophorian Ciliates (Ciliophora, Cyrtophoria) from China

“…Sequence selection and alignment, and phylogenetic tree construction methods are described in the Supplementary Materials . The topology of the present phylogenetic tree is consistent with previous works (e.g., [ 14 , 41 , 59 , 77 , 78 , 79 , 80 , 81 , 85 , 88 , 89 , 90 ]), and similar conclusions can be drawn: (1) The order Clamydodontida are monophyletic, while the order Dysteriida are non-monophyletic. (2) The subclass Chonotrichia are nested within Dysteriida, on the level of the family Hartmannulidae.…”

“…Other works involving molecular phylogeny (SSU rDNA) were combined with morphological descriptions, serving as a complementary method for species identification [ 12 , 13 , 14 , 24 , 25 , 26 , 37 , 39 , 41 , 59 , 74 , 77 , 78 , 79 , 80 , 81 ].…”

“…Similarly, although Gastronautidae has only one sequence positioned within the family Chilodonellidae, this family is valid and represents an intermediate group within the order Chlamydodontida based on its unique combination of morphological characteristics [ 14 ]. The separation of Kyaroikeidae ( Kyaroikeus and Planilamina ) from Dysteriidae is not well supported by either morphological or molecular data, and Kyaroikeidae species could be seen as highly specialized Dysteriidae adapted to parasitism [ 41 ]. Therefore, we place it at the basal position of Dysteriidae.…”

“…Several free-living species thrive in mariculture [ 33 , 34 , 35 ] and freshwater fish aquaculture tanks [ 36 ]. A few species even live as obligate parasites on the gills and skin of fish [ 36 , 37 , 38 , 39 , 40 ], or on the mucosa of the blowholes of sea mammals [ 41 , 42 , 43 ], and hence are target organisms in pathogenic studies [ 44 ].…”

A Case Study of the Morphological and Molecular Variation within a Ciliate Genus: Taxonomic Descriptions of Three Dysteria Species (Ciliophora, Cyrtophoria), with the Establishment of a New Species

“…Cyrtophorians are highly divergent ciliates with dorsoventrally or laterally flattened bodies. Since the beginning of the 21st century, numerous cyrtophorians have been reported from various habitats, and many of these have been used as model organisms in morphological and genetic diversity research [1,5,10,12,[18][19][20][21][22]. Dysteria Huxley, 1857, is a specialized cyrtophorian genus with a highly bilaterally compressed body and somatic cilia densely arranged in kineties that are restricted to a narrow ventral groove between two lateral plates.…”