Botryllus schlosseri

BRIEF HISTORICAL ACCOUNT OF THE SPECIES

 

The second half of the XVIII century represented the golden age for both intellectual curiosity and studies on the knowledge of the marine and lagoon fauna and flora in a very lively cultural climate, involving European physicians, abbots, philosophers and naturalists. In such time, various researchers, graduated or not, undertook investigations on the marine biology the aim of which, as well as the physiology and morphology together with the geological and mineralogical studies, was the outlining of a map of the resources of the Mediterranean basin. The lagoon of Venice and the Northern Adriatic Sea were object of investigation of various naturalists of Chioggia and the splendour of their researches reflected on the entire Venetian Region and Europe. The first best picture of an animal referable at present with a colony of Botryllus schlosseri is a drawing of 1784 by the naturalist Stefano Chiereghin (Chioggia, 1745-1820). It was made in two different life moments following the development and transformations within 48 hours of a colony collected in the lagoon of Venice. The drawing supports the description of a "new animal -  zoophyton" in the scientific diary namely Giornale (Journal), that Lazzaro Spallanzani (Reggio Emilia 1729 -  Pavia 1799), sublime naturalist and pioneer of the experimental biology, wrote when explored the gulf of Venice from the half of August to the end of October in 1784, within a wider and ambitious plan, the Storia naturale del mare (Natural history of the sea), never published. Note that, besides the very detailed drawing of Chiereghin, in this description Spallanzani described for the first time changing and behaviour of the colony.

"20 August 1784. This morning a new phenomenon is happened. The zoophyton collected yesterday and left always in seawater did not show only 6 leaves but 12. In one day, 6 new leaves formed very similar to the old ones. The zoophyton was circular and now it is still in such shape. However, the animal seems to be dead because the leaves are disarranged and do not show any motion when they are stung. I don't  know if the animal was disarranged since it was at the end of its life or it was in an inadequate place."

Nevertheless, Spallanzani did not recognised in this zoophyton the plant-animal described for the first time by John Albert Schlosser and John Ellis in Philosophical Transactions (Vol. XLIX) of the Royal Society (1755-1756) (Schlosser: "A coral-like substance", page 449; Ellis: "Remarks on the same", page 452) for specimens kept in alcohol, that Peter Simon Pallas in the Elenchus zoophytorum (1766) and Carl von Linné in the XIII edition of  Sistema Naturae (1770) then denominated Alcyonium schlosseri Linn. in his honour: "Alcyonium subrotundum stuposum, stellis radio pertusis".

 About the end of the XVIII century, the naturalists realised that, with the Alcyonium term, soft, gelatinous and compound organisms at the boundary between the animal and the vegetable kingdom (Plantanimalia) were actually grouped with characteristics very different among them. In a letter to Pallas, J. Gaertner proposed of changing the name of the species with Botryllus stellatus. Pallas, in Spicilegia Zoologica fasc. X (1774), reported in turn the drawing and the description of Gaertner recognising that it must form a new genus. From then, all the history of the present classification followed enclosing the synonymized taxa due to the chromatic polymorphism typical of this species:

 In 1792, Giuseppe Olivi (Chioggia 1769 -  Padova 1795) reported some interesting scientific observations on Alcyonium schlosseri in his volume Zoologia Adriatica, first of all recognising the new genus Botryllus.

 "It lives in the lagoons and in the shallow waters along the coasts, covering the stipes of Zostera and many other vegetable and animal organisms. The description of Gaertner agrees exactly with the specimens of our sea".

 As the first one, this young naturalist who died prematurely and to whom the Museum of Adriatic Zoology in Chioggia is dedicated, recognised the presence, the sensitiveness and the role of the siphons.

 "When one of the numerous small mouths forming the star is stimulated the small mouths do not contract. On the contrary, they close all together when the central part of the star is stimulated. […] These stars are not a single organism but a polyp with many heads sprouting new small heads. I don't  agree with Gaertner that the small mouths of the rays of the stars are heads […], but they are openings for absorbing the foods and conveying the feeding to the centre of the star".

 In a letter (Sopra il Botrillo piantanimale marino) sent to Olivi in 1793 Stefano Andrea Renier (1759-1830), future teacher of Natural History at the University of Padova, reported the results of the first zootomy observations carried out on a specimen of B. schlosseri.

 

B. schlosseri AS A MODEL SPECIES OF THE XXI CENTURY: A STAR IS BORN (click on)

Ascidians are sessile, filter-feeding marine organisms with worldwide distribution representing the largest class in the subphylum Tunicata or Urochordata, which is phylogenetically close to vertebrates. Belonging to the phylum Chordata, tunicates, during larval stage, share with vertebrates the same body plan (dorsal notochord and a tubular nervous system, both flanked by striated muscle, a pharynx with gill slits and a ventral heart); moreover their nervous system is patterned by developmental genes common to vertebrates. Ascidians are the closest relatives to vertebrates, and are the only chordates able to reproduce both sexually and asexually. For these reasons, both solitary and colonial ascidians are the most intensively studied tunicates.

 Scheme of the internal anatomy of a  B. schlosseri colony

(modified from Delage Y. and Hérouard E., 1898, Traité de Zoologie Concrète. Schreicher Fréres Eds., Paris)

 

The star ascidian Botryllus schlosseri is an ubiquitary compound ascidian, easy to collect and rear in aquaria, introduced in our lab as a model organism more than 50 years ago by Prof. Armando Sabbadin, at the University of Padova, who for the first time set up conditions for the permanent culture of this species, which had only occasionally been reared before, mainly due to interest in its budding.

 It is now emerging as a simple and important model species for the study of a variety of biological processes, such as immunobiology, allorecognition, sexual and asexual reproduction, differentiation, regeneration, stem cell differentiation, apoptosis, angiogenesis, development of nervous system, presence and fate of placodes and neural crests.

 Since 2013, its genome is available at Botryllus schlosseri Genome Project (Ref.: Voskoboynik et al., 2013).

 This species forms colonies through asexual reproduction (palleal budding), in which 5-10 adult zooids are organised in star-shaped systems and embedded in a thin transparent extracellular collagenous matrix (the tunic) containing numerous scattered cells.

B. schlosseri colonies are formed of hundreds adult clonal zooids, all genetically identical, and each colony presents at any time three coordinated generations: adults, bud, and budlets. Weekly, at the temperature of 18 °C, a generation change occurs during which the adults die, and are resorbed, while their buds reach functional maturity becoming the new adults. At the same time their buds produce new budlets. During the regular changes of generation, massive apoptosis occurs.

 B. schlosseri offers several advantages as an experimental organism:

Taking advantage of these features, blastogenesis has been studied by means of several kinds of experimental approach. For example, thanks to the tunic features and bidimensional arrangements of zooids, it is possible not only to select colonies at specific developmental stages, but also to operate on them with a thin, tungsten needle (e.g., to remove zooids of different generations from a system, to damage them, isolate them from other individuals or from the vascular net, graft buds on to the tunic, and so on). This kind of experimental procedure was first introduced by Sabbadin in 1956 and then adopted by many researchers to study bud regeneration, regulation of programmed cell death and cell removal during take-over and relationships between the resorption of old zooids and bud growth, establishment of bud axes during development, and competition between different generations in the colony. The differential ability of zooids to survive and resume the colonial life cycle in varying experimental conditions has revealed that colonies have a great regulative potential, which manifests itself in differing ways, for example, with anticipation of regression of filtering adults, whose components can be re-used by growing buds, and variations in zooid growth rate, duration of zooid life span, and budding intensity.

Botryllus possesses two reproductive modes: sexual reproduction with ovoviviparity (embryogenesis), commonly used for dispersion of individuals with re-assorted new genomes, and asexual reproduction (blastogenesis), for formation of colonies with many individuals. These two different modes of reproduction present common and divergent aspects. Despite the different origin of the germ layers of bud and embryos, the two developmental pathways lead to adults with a similar morphology. Molecular and cellular evidences support the idea that homologies exist in the development, not only between embryo and bud, but also between tunicates and vertebrates.

Botryllus has a colonial circulatory system (CCS), composed by an intricate network of anastomised vessels external to zooids and embedded in the tunic, that possesses an incredible regenerative potential, as shown by its ability to reform tunic and peripheral vascular network. Vessel regeneration occurs mainly by the same angiogenic sprouting mechanism with participation of the same growth factors of the vertebrate circulatory system during normal growth and in regenerating organs and tumours. In addition, when all the zooids of a colony are experimentally ablated, the CCS can trigger an alternative way of asexual reproduction (vascular budding), giving rise to adult complete zooids starting from evaginations of the vascular epithelium that incorporate blood stem cells.