Towards a Molecular Systematics of the Lake Baikal/Lake Tuva Sponges

Abstract

Lake Baikal is famous for its extensive biodiversity that is equaled only by few other lakes. Fascinatingly, about 80% of all the animals the lake hosts are endemic. Sponges (Porifera) that live in symbiosis with photosynthetic algae are the most abundant animal taxon found in the littoral zone of Lake Baikal and have been grouped to the family Lubomirskiidae. In recent years, several attempts to determine the phylogenetic relationship between Lubomirskiidae and cosmopolitan freshwater sponges have been undertaken. Yet the results obtained remain inconclusive. Here, we strive to determine the phylogeny of freshwater sponges with the focus on endemic Lake Baikal species, also taking into account two poriferan species that were collected during an expedition in 2006 in two other isolated Siberian lakes, Lake Chagytai and Lake Tore-Khol. Since its discovery at the beginning of the twentieth century, the Lake Chagytai species was grouped to the Lubomirskiidae and called Baikalospongia dzhegatajensis. However, analyses of molecular sequence data [internal transcribed spacer 2 (ITS2), ribosomal DNA (rDNA)] and morphological markers (spicules, habitus) inferred a close relationship to the cosmopolitan genus Ephydatia and also to the Lake Tore-Khol species that had not so far been described. Thus, both species were tentatively termed Ephydatia tuva (Lake Chagytai) and E. altaiensis (Lake Tore-Khol). We hypothesize that these new species might have evolved from Ephydatia-like ancestors through adaptation to the unique environmental conditions of both lakes. To test the ITS data, an unlinked genetic locus was chosen for further phylogenetic analyses, the protein-coding gene silicatein. These analyses provided not only a more robust resolution between the Lubomirskiidae, but also corroborated the grouping of the Lake Chagytai and Lake Tore-Khol species to the genus Ephydatia. In addition, the phylogenetic analyses suggest a Spongilla-like founder generation of poriferan species in Lake Chagytai and Lake Tore-Khol. In conclusion, we propose that the process of speciation in Lake Baikal and Lake Chagytai/Lake Tore-Khol, from a cosmopolitan Spongilla-like ancestor to more than ten endemic species follows allopatric speciation patterns and is of the peripatric type.

Acquisition of Structure-guiding and Structure-forming Properties during Maturation from the Pro-silicatein to the Silicatein Form

“…E-64 inhibited directly the processing of the cathepsin-related silicatein, as expected (data not shown) (31), while the maturation of prosilicatein to silicatein proceeded in the presence of PMSF. PMSF is known to be an effective inhibitor of thrombin protease (39), however, only for a very limited period of time (about 1 h) (32) and surely not for 24 h as seen in our assays 3 . Therefore, we have strong reasons to assume that the processing of pro-silicatein to silicatein is the result of an autocatalytic reaction.…”

“…Silicatein cleavage has been proposed to proceed either by autolysis (29) or by a second protease (30). Since the processing of the S. domuncula pro-silicatein-␣ to silicatein-␣ can be prevented by the incubation with 5 M E-64 3 , an irreversible inhibitor of a wide range of cysteine peptidases, including silicatein from the hexactinellid Monorhaphis chuni (31), an autocatalytic cleavage process is most likely.…”

“…Their morphologies, sizes, and shapes are characteristic for each sponge species (2), and in turn their synthesis is primarily genetically controlled (3). The spicules in sponges are formed either of silica, like in the classes Hexactinellida and Demospongia, or of calcite, like in the class of Calcarea (1).…”

The Role of Proteins in Biosilicification

“…The axial filaments survive the harsh extraction procedure (though they can be denatured by boiling [83]) and are able to catalyze formation of insoluble silica from organosilanes like tetraethoxysilane (which is otherwise stable in water), leading to precipitation along the filaments' long axis and 29 Si-NMR evidence for an incompletely polymerized silica network [83]. Silicatein-like proteins have also been discovered in many other sponges [84] including proteins in the ratio 4 silicatein α  : 1 silicatein β in Suberitus domuncula [85], a dimerizing silicatein in Petrosia ficiformis corresponding to silicatein β [86], and even silicateins from nonspicule forming sponges [87]. Many of these silicatein-producing sponges come from Lake Baikal which continues to be a rich source of diversity amongst the siliceous sponges [88, 89].…”

The endemic Cladophorales (Ulvophyceae) of ancient Lake Baikal represent a monophyletic group of very closely related but morphologically diverse species

“…2012, Semernoy 2004, Seehausen 2006, Albrecht and Wilke 2008, Glaubrecht and von Rintelen 2008, Wiens et al 2009, Shirokaya et al 2017. It is striking that to date species flocks in ancient lakes have been reported almost exclusively for animal taxa and for no algal or plant group except diatoms (Mann 1999, Flower 2005, Edlund and Soninkhishig 2009, Kulikovskiy et al 2012.…”