Carnivorous sponges of the Atlantic and Arctic Oceans. Phylogeny, taxonomy, distribution and microbial associations of the Cladorhizidae (Demospongiae, Poecilosclerida)
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The sponges (phylum Porifera) are defined by the presence of an aquiferous system in which choanoflagellate cells create a current and filter water flowing through the sponge body. The carnivorous sponges represent the only known exception to filter feeding within the phylum, and instead are able to capture prey including small crustaceans and larval plankton, using a combination of an adhesive surface and numerous filaments suitable for entangling prey. Mobile cells are able to slowly cover prey entangled on the surface of the sponge, and prey items are encapsulated and digested in a process that can last several days. The aquiferous system is either strongly reduced or entirely absent in the carnivorous sponges, which typically have an erect pennate, branching or stipitate pedunculate morphology. Carnivory is usually considered an adaptation to deep-sea conditions, where filter feeding is less efficient due to a lower density of suspended particulate matter. An exceptional evolutionary innovation within the phylum, sponge carnivory was not properly known to science until 1995. Interest in carnivorous sponges have been high in recent years, and over 150 species are currently considered valid, up from some 90 known species at the turn of the millennium. Carnivorous sponges are found within the demosponge order Poecilosclerida, defined by the presence of skeletal chela microsclere spicules. Almost all carnivorous sponges have traditionally been assigned to Cladorhizidae, with a few species assigned to Guitarridae (Euchelipluma) and Esperiopsidae (five Esperiopsis spp.). As spicule morphology is the main diagnostic character in sponge systematics, the large diversity of chela forms found within the genera assigned to Cladorhizidae implies the possibility that the family is polyphyletic, and that carnivory has evolved in several independent poecilosclerid lineages. On the other hand, recent molecular studies have shown that spicule morphology is often more plastic and intricate than previously believed. Thus the question of whether carnivorous sponges represent a monophyletic group is currently unanswered. Recent studies have greatly expanded the number and known distribution of carnivorous sponges, which are now known to be present at a variety of depths worldwide. Still, as deep-sea sponges, records are comparably sparse. The greatest number of records is from the North Atlantic. However, records are scattered, and species descriptions frequently lacking in detail. In other areas of the Atlantic and worldwide, species are typically known only from a few or even one collection event. As they have an affinity to the deep sea, carnivorous sponges are often reported in the vicinity of vent and seep sites. In one particular instance, chemoautotrophic symbiosis has been reported between the carnivorous sponge Cladorhiza methanophila and methanotrophic prokaryotes from the Barbados Accretionary Prism. The extent of this type of symbiosis within the group is unknown, however, and though general sponge microbiome data is increasingly published as NGS studies have become more prevalent, almost no such data is currently published for carnivorous sponges. Answering a number of current questions connected to carnivorous sponges, the aims of this thesis include (1) elucidating the systematic relationships of the carnivorous sponges using molecular data, (2) presenting a taxonomic inventory of carnivorous sponges focusing on Atlantic species, and (3) conducting a comparative study of the microbial community of several cladorhizid species including C. methanophila using mainly 16S rRNA Ion Torrent data. The work presented here provides a comprehensive phylogenetic analysis containing representatives of almost all carnivorous sponge groups, including species not traditionally included in Cladorhizidae, as well as an outgroup sampling of noncarnivorous relatives. The phylogenetic study is able to show that carnivorous sponges represent a monophyletic group, strengthening the hypothesis that carnivory only has evolved once within the sponges, and assigning all carnivorous sponges to Cladorhizidae. Furthermore, this work shows the position of Cladorhizidae relative to other poecilosclerid families, and is able to reconstruct cladorhizid relationships at the genus and subgenus level in most cases. Using an integrated taxonomical approach, molecular data and morphological characters are combined to create an updated classification for all known carnivorous sponges. The thesis adds to, and includes an overview of the known cladorhizid species diversity in different regions of the Atlantic Ocean. It offers a comprehensive overview of the cladorhizid fauna of the boreal North Atlantic and Arctic, including descriptions of 25 species and an overview of their known distributions, and explores the cladorhizid fauna of the abyssal Atlantic and Caribbean and adjacent areas respectively. A summary of known carnivorous sponges for the Atlantic Ocean in general, with a discussion on the relationships of the regional Atlantic faunas, is also presented, as well as observations on the depth preference of different species. Finally, this thesis also presents a comparative examination of 16S rRNA microbiome and isotope data from several carnivorous sponge species including Cladorhiza methanophila. Results show that cladorhizid sponges have rich microbial communities, which partially overlap between species. No further evidence of major chemoautotrophic symbiosis was found in species other than C. methanophila, where methanotrophic bacteria were abundant, suggesting that this species is likely an exception within carnivorous sponges in general. There is currently a high degree of interest in carnivorous sponges. As more morphological, molecular and biogeographic data is published, refinements to both the systematics, taxonomical diversity, function and ecology of this group are expected, further building on the results presented in this thesis and giving a more complete picture of the known diversity, evolutionary history and biogeography of the Cladorhizidae.
Has partsPaper I: Hestetun JT, Fourt M, Vacelet J, Boury-Esnault N, Rapp HT (2015). Cladorhizidae (Porifera, Demospongiae, Poecilosclerida) of the deep Atlantic collected during Ifremer cruises, with a biogeographic overview of the Atlantic species. Journal of the Marine Biological Association of the United Kingdom 95(7), 1311-1342. The article is not available in BORA due to publisher restrictions. The published version is available at: https://doi.org/10.1017/s0025315413001100
Paper II: Hestetun JT, Pomponi S, Rapp HT. The cladorhizid fauna (Porifera, Poecilosclerida) of the Caribbean and adjacent waters. Zootaxa 4175(6), 521-538. The article is available at: http://hdl.handle.net/1956/15239
Paper III: Hestetun JT, Tompkins-MacDonald G, Rapp HT. A review of carnivorous sponges (Porifera: Cladorhizidae) from the boreal North Atlantic and Arctic. The article is not available in BORA.
Paper IV: Hestetun JT, Vacelet J, Boury-Esnault N, Borchiellini C, Kelly M, Ríos P, Cristobo J, Rapp HT (2016). The systematics of carnivorous sponges. Molecular Phylogenetics and Evolution 94, 327-345. The article is available in the main thesis. The published version is also available at: http://dx.doi.org/10.1016/j.ympev.2015.08.022
Paper V: Hestetun JT, Dahle H, Jørgensen SL, Olsen BR, Rapp HT. The microbiome and occurrence of methanotrophy in carnivorous sponges. Frontiers in Microbiology 7, 1781. The article is available at: http://hdl.handle.net/1956/15240