Genetics and Morphology Characterize the Dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the Sole Representative of Symbiodinium Clade E

Abstract

Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture them often retrieve isolates that may not be symbiotic, but instead exist as free-living species. In particular, cultures of Symbiodinium clade E obtained from temperate environments were recently shown to feed phagotrophically on bacteria and microalgae. Genetic, behavioral, and morphological evidence indicate that strains of clade E obtained from the northwestern, southwestern, and northeastern temperate Pacific Ocean as well as the Mediterranean Sea constitute a single species: Symbiodinium voratum n. sp. Chloroplast ribosomal 23S and mitochondrial cytochrome b nucleotide sequences were the same for all isolates. The D1/D2 domains of nuclear ribosomal DNA were identical among Western Pacific strains, but single nucleotide substitutions differentiated isolates from California (USA) and Spain. Phylogenetic analyses demonstrated that S. voratum is well-separated evolutionarily from other Symbiodinium spp. The motile, or mastigote, cells from different cultures were morphologically similar when observed using light, scanning, and transmission electron microscopy; and the first complete Kofoidian plate formula for a Symbiodinium sp. was characterized. As the largest of known Symbiodinium spp., the average coccoid cell diameters measured among cultured isolates ranged between 12.2 (± 0.2 SE) and 13.3 (± 0.2 SE) μm. Unique among species in the genus, a high proportion (approximately 10-20%) of cells remain motile in culture during the dark cycle. Although S. voratum occurs on surfaces of various substrates and is potentially common in the plankton of coastal areas, it may be incapable of forming stable mutualistic symbioses.

Symbiodinium necroappetenssp. nov. (Dinophyceae): an opportunist ‘zooxanthella’ found in bleached and diseased tissues of Caribbean reef corals

“…The detection and genetic analysis of Symbiodinium from water samples, sediments and various other substrata reveals the existence of unusual genetic lineages not detected in host tissues and signifies the existence of a diverse group of 'freeliving', opportunistic and possibly non-mutualistic species (LaJeunesse, 2002;Hirose et al, 2008;Porto et al, 2008;Pochon et al, 2010;Jeong et al, 2014). These and other findings have led to the growing realization that the ecological breadth of the genus Symbiodinium extends well beyond endosymbiotic mutualisms (LaJeunesse, 2001(LaJeunesse, , 2002Lesser et al, 2013;Jeong et al, 2014).…”

“…These and other findings have led to the growing realization that the ecological breadth of the genus Symbiodinium extends well beyond endosymbiotic mutualisms (LaJeunesse, 2001(LaJeunesse, , 2002Lesser et al, 2013;Jeong et al, 2014). Some have presumed that members of Clade A (sensu lato) are stress tolerant, fugitive opportunists and even parasites (Toller et al, 2001;Stat et al, 2008;Lesser et al, 2013).…”

Morphological characterization of Symbiodinium minutum and S. psygmophilum belonging to clade B

“…The cells from much information on their taxonomy is available. In particular, the morphological characters of Symbiodinium have been studied much less than their genetic characters (Kevin et al 1969, Loeblich and Sherley 1979, Santos et al 2003, Coffroth and Santos 2005, Hansen and Daugbjerg 2009, Jeong et al 2014a) because of their difficulty in culturing and scanning electron microscopy (SEM) observations. Thus, some newly established Symbiodinium species provided only genetic information without morphological information.…”

“…The genus Symbiodinium comprises nine clades (Rowan and Powers 1992, Pochon and Gates 2010), which are phylogenetically divergent and differ in global distributions as well as abundances (Jeong et al 2014a). The Symbiodinium species belonging to clade B have been found inside sea anemones and corals (Rowan and Knowlton 1995, Diekmann et al 2003, LaJeunesse et al 2012 minutum was x, EAV, 4ʹ, 5a, 8ʹʹ, 7s, two cingulum rows, 18-20c, 5-6ʹʹʹ, and 2ʹʹʹʹ ( (Fig.…”

“…The genus Symbiodinium, commonly known as zooxanthellae, comprises symbiotic dinoflagellates, most of which are symbiotic with various species such as corals, sponges, sea anemones, jellyfish, nudibranchs, clams, ciliates, and foraminifera (LaJeunesse 2002, RodriguezLanetty et al 2003, Lewis and Coffroth 2004, Fay et al 2009, Pochon and Gates 2010, Hill et al 2011, Pochon et al 2012, although some exist as free-living forms (Gou et al 2003, Hansen and Daugbjerg 2009, Jeong et al 2012, 2014a, 2014b. They are crucial components of coral reef ecosystems (Iglesias-Prieto et al 1992, Stanley 2006, Stat et al 2006; however, despite their ecological importance in marine ecosystems, not izations such as plate tabulations and related diagnoses have not been provided (LaJeunesse et al 2012).…”