Parvilucifera multicavata sp. nov. (Alveolata, Perkinsozoa), a New Parasitoid Infecting Marine Dinoflagellates Having Abundant Apertures on the Sporangium

The phylum Perkinsozoa is known as an exclusively parasitic group including the parasites of shellfish, fish, dinoflagellates, cryptophytes, and tadpoles and at present comprises seven genera across three families (Parviluciferaceae, Perkinsidae, and Xcellidae), with the genus Parvilucifera having the most abundant species in the family Parviluciferaceae. During intensive sampling along the Korean coast in August and September 2017, a new species of the genus Parvilucifera was discovered and successfully established in cultures. Morphological and ultrastructural observations revealed that the new parasitoid shares almost all known diagnostic characters with other species of Parvilucifera, except that its sporangium has a higher number of apertures although with smaller diameters than those in P. infectans. Molecular phylogenetic trees based on both nuclear small subunit (SSU) and concatenated SSU and large subunit (LSU) ribosomal DNA (rDNA) sequences revealed that the new parasitoid was nested within the family Parviluciferaceae and had a sister relationship with P. infectans. Based on morphological, ultrastructural, and molecular data, we propose to erect a new species, P. multicavata sp. nov., for the new parasitoid found in this study.

Introduction

The phylum Perkinsozoa is an exclusively parasitic group (Norén et al. 1999), including Perkinsus, which infects shellfish (Levine 1978), Rastrimonas subtilis, which infects cryptophytes (Brugerolle 2002), the family Xcellidae, which is a fish parasite (Freeman et al. 2017), and the family Parviluciferaceae, which infects dinoflagellates (Reñé et al. 2017a). Although the morphology is not formally described, the small subunit (SSU) ribosomal DNA (rDNA) sequences of parasites causing mass-mortality events of tadpoles are also placed within the Perkinsozoan clade in the phylogenetic tree (Chambouvet et al. 2015). In addition, numerous unidentified environmental sequences affiliated with Perkinsozoan parasites from freshwater, seawater, sediment, hydrothermal vents, and peat bogs have also been detected (Behnke et al., 2010, Bråte et al., 2010, Chambouvet et al., 2014, Lara et al., 2011, López-García et al., 2003). Among the perkinsozoan parasites in particular, the number of species belonging to the family Parviluciferaceae has greatly increased over the last decade. The family at present comprises four genera: Dinovorax, Snorkelia, Tuberlatum and Parvilucifera. The first two genera (i.e., Dinovorax and Snorkelia) have a characteristic morphology of the sporangium, whose surface is smooth and has only one long germ tube (1:1.6–1.8; mean ratio of germ tube length relative to sporangium diameter) (Reñé et al. 2017a). By comparison, the sporangium of Tuberlatum also has a smooth surface; however, it is characterized by the presence of two to four distinct dome-shaped, short germ tubes (1:8; mean ratio of germ tube length relative to sporangium diameter) (Jeon and Park 2019). In contrast, the sporangium of Parvilucifera does not have any short or long germ tube(s). Instead, it is covered by numerous processes on the surface and has several opercula and apertures, from which the newly produced zoospores are released (Figueroa et al., 2008, Jeon et al., 2018, Lepelletier et al., 2014, Norén et al., 1999, Reñé et al., 2017b).

Unlike other genera (i.e., Dinovorax, Snorkelia, and Tuberlatum) having only one species in each genus, Parvilucifera has the most abundant number of species in the family Parviluciferaceae, including P. infectans, P. sinerae, P. prorocentri, P. rostrata, and P. corolla (Figueroa et al., 2008, Leander and Hoppenrath, 2008, Lepelletier et al., 2014, Norén et al., 1999, Reñé et al., 2017b). Considering the marked morphological differences and phylogenetic distance, however, P. prorocentri was recently moved into a new genus Snorkelia (Reñé et al. 2017a). The two species P. infectans and P. sinerae, which are very similar or almost identical morphologically and genetically (Figueroa et al., 2008, Lepelletier et al., 2014, Norén et al., 1999), have long been considered different species (e.g., Figueroa et al., 2008, Garcés and Hoppenrath, 2010) but are revealed to be the same species when based on a set of morphological, ultrastructural, and molecular data (Jeon et al. 2018). Consequently, three species, P. infectans, P. rostrata, and P. corolla, now remain valid in the genus Parvilucifera.

During intensive sampling along the Korean coast in August and September 2017, a new species of Parvilucifera was discovered, and two strains of the new species were successfully established in cultures. Light and electron microscopy were used to characterize the life cycle stage, morphology, and the ultrastructure of the new species Parvilucifera multicavata sp. nov. The phylogenetic position of the new species was also presented with other species of the family Parviluciferaceae as well as numerous environmental sequences within Perkinsozoa.