Ultrastructure and formation of the body cavity lining in Phoronis muelleri (Phoronida, Lophophorata)

Abstract

Among other characteristics a trimeric coelomic compartmentation consisting of an anterior protocoel, followed by a mesocoel and a posterior metacoel is traditionally believed to substantiate the sister-group relationship between Lophophorata and Deuterostomia, together forming the Radialia. As molecular data cannot support this hypothesis a reanalysis of the coelomic cavities in Phoronida is undertaken, because corresponding coelomic compartmentation is widely accepted to support the Radialia hypothesis. A coelomic cavity can be recognized on the ultrastructural level because its lining is a true epithelium with polarized cells interconnected by apical adherens junctions. This study reveals that neither in larval nor adult Phoronis muelleri (Phoronida) an anterior cavity with such a lining is present. What on the light microscopic level leads to the impression of a cavity inside the larval episphere, actually is an enlarged subepidermal extracellular matrix with an amorphous, presumably gel-like filling, into which several muscle cells are embedded. Larvae, thus, possess only one coelomic cavity, the large trunk coelom of the larva which is adopted in the adult organization. The second coelomic cavity of adult P. muelleri, the lophophore coelom, develops as a double-layer of epithelialized mesodermal cells at the base of the adult tentacle buds and becomes fluid filled during metamorphosis. Like the larval episphere, larval tentacles and most parts of the blastocoel are filled by an amorphous matrix. Reanalysis of the literature and comparison with Brachiopoda and Bryozoa allows the hypothesis that a protocoel is lacking in all Lophophorata, and that merely two unpaired coelomic cavities, one tentacle and one trunk coelom, can be assumed for the ground pattern of this taxon. These results do not provide further evidence for the Radialia hypothesis, but also do not contradict it. 1 The nominal name Actinotrocha J. Müller, 1846 is a senior synonym of Phoronis Wright, 1856; the specific name Actinotrocha branchiata J. Müller, 1846 is a senior synonym of Phoronis muelleri Selys-Longchamps, 1903. According to the IRZN Articles 23.2 and 23.9 prevailing usage must be maintained: Phoronis and Phoronis muelleri are the valid names for the taxa in question.

Phylogenomic analyses of lophophorates (brachiopods, phoronids and bryozoans) confirm the Lophotrochozoa concept

“…However, in the last decade, the morphological evidence for a close relationship between the lophophorate groups and the deuterostomes has become weaker by careful re-examinations of the characters. It has been shown that neither brachiopods nor phoronids possess three coelomic cavities, because a protocoel is lacking in all lophophorate groups (Lü ter 2000; Bartolomaeus 2001). Thus, the archicoelomate concept (Siewing 1980) uniting Lophophorata and Deuterostomia, founded on the similarities of three distinct coelomic cavities, lost its basis.…”

Ultrastructure of the body cavities in Phylactolaemata (Bryozoa)

“…However, no coelom but only ECM and isolated muscle cells are found in these structures (Lü ter, 1996(Lü ter, , 2000. In Phoronis muelleri as well as in Phoronis ovalis, the epistome does not contain a coelomic cavity, but only ECM and muscle processes (Bartolomaeus, 2001;Gruhl et al, 2005).…”

“…In contrast to such far-reaching hypotheses, the organ itself remained relatively poorly studied. In Phoronida as well as Brachiopoda, ultrastructural studies have found no support for a separate coelomic cavity in the epistome in representatives of these taxa (Lü ter, 1996;Bartolomaeus, 2001;Gruhl et al, 2005), although this had been suggested by earlier investigations (e.g., Siewing, 1973;Emig and Siewing, 1975;Herrmann, 1980;Zimmer, 1980). In phylactolaemate bryozoans, there is clearly no evidence for a tripartion of the coelom at any time during embryonic development (Mukai, 1982;Nielsen, 2001).…”

Phoronida

“…Each of these body regions was originally described as having a true coelomic cavity lined by mesoderm and were interpreted as the protocoel (epistome), mesocoel (lophophore), and metacoel (trunk), linking this arrangement to the tripartite coeloms found in echinoderms (Masterman 1898 ). The epithelial lining of the epistome in two species of Phoronis was found instead to be myoepithelial cells lacking adherent junctions surrounding a gel-like extracellular matrix, thus not exhibiting the features of a true epithelial layer (Bartolomaeus 2001 ;Gruhl et al 2005 ). Further complicating these fi ndings are ultrastructural observations of the epistome lining of Phoronopsis harmeri , which does contain adherent junctions (Temereva and Malakhov 2011 ).…”

“…These cells will form a small cavity underneath the apical tuft region of the late gastrula. This cavity has been interpreted as the fi rst coelomic cavity ("protocoel"), but as discussed previously, whether these cells form a true epithelium in all or in just select species is debated (Zimmer 1978 ;Bartolomaeus 2001 ;Temereva and Malakhov 2006 ). At this asymmetric late gastrula stage, the gut is a blind sac.…”