Characterisation of sphaeractinomyxon types (Cnidaria: Myxozoa) from marine and freshwater oligochaetes in a Portuguese estuary, with the demise of the endocapsa collective group

Abstract

Six types of sphaeractinomyxon are reported from the coelomic cavity of oligochaetes collected from the Minho River estuary in northern Portugal. Four new types are morphologically and molecularly described from freshwater species belonging to the genera Psammoryctides Hrabě and Potamothrix Vejdovský et Mrázek in the upper estuary, thus significantly increasing the number of known freshwater sphaeractinomyxon. In the lower estuary, sphaeractinomyxon types 8 and 10 of Rangel et al. (2016) are recorded infecting the marine oligochaete Tubificoides pseudogaster (Dahl). A single specimen of T. pseudogaster further displayed infection by one of the four new types found in the upper estuary, suggesting the involvement of sphaeractinomyxon in the life cycles of myxosporean species that infect migratory fish hosts. The acquisition of these second hosts is proposed to have allowed the myxosporean counterparts of sphaeractinomyxon to cross environmental barriers and conquer new habitats. Phylogenetic analyses of the SSU rRNA gene reveal the four new types clustering within the monophyletic clade of mugiliform-infecting myxobolids, strengthening the previously proposed involvement of the sphaeractinomyxon collective group in the life cycles of this specific group of myxosporeans. Endocapsa types also cluster within the latter clade, having actinospores that differ from those of sphaeractinomyxon only in the presence of valvular swellings that do not change when in contact with water. In this study, however, one type was found displaying actinospores with and without valvular swellings in the same oligochaete specimen. This overlap in actinospore morphology is given as grounds for the demise of the endocapsa collective group.

Involvement of sphaeractinomyxon in the life cycle of mugiliform-infecting Myxobolus (Cnidaria, Myxosporea) reveals high functionality of actinospore morphotype in promoting transmission

“…Sphaeractinomyxon types genetically more similar were the Sphaeractinomyxon type 1 of Rocha et al . (2020) (MK418446) (94.2%) and the Sphaeractinomyxon type 1 of Rocha et al . (2019 c ) (MH017876) (94.0%).…”

“…Acknowledging the widely reported artificiality of using morphological criteria for distinguishing between members of sphaeractinomyxon (Rangel et al, 2016b;Rocha et al, 2019cRocha et al, , 2020, and other actinospore collective groups in general (e.g. Hallett et al, 2002Hallett et al, , 2004Eszterbauer et al, 2006;Caffara et al, 2009;Xi et al, 2015), differentiation between the four new types was mainly based on molecular data of the SSU rDNA gene.…”

“…In the case of sphaeractinomyxon, 32 types (including former tetraspora and endocapsa representatives) have been reported from either freshwater or marine oligochaetes (Marques, 1984; Hallett et al ., 1997, 1998, 1999, 2001; Hallett and Lester, 1999; Rangel et al ., 2016 b ; Rocha et al ., 2019 c , 2020). In fact, more than half of these types were described from Portuguese estuaries, mainly from infections in the marine oligochaetes Limnodriloides agnes Hrabě, 1967 (Oligochaeta, Naididae), Tubificoides pseudogaster (Dahl, 1960) (Oligochaeta, Naididae) and Tubificoides insularis (Stephenson, 1923) (Rangel et al ., 2016 b ; Rocha et al ., 2019 c , 2020). Four types were reported to occur in freshwater, infecting Psammoryctides barbatus (Grube, 1861) (Oligochaeta, Naididae), and an unidentified species of the genus Potamothrix Vejdovský and Mrázek, 1903 (Oligochaeta, Naididae); this included one type that was also molecularly shown to occur in the marine oligochaete T. pseudogaster (Rocha et al ., 2020).…”

“…In fact, more than half of these types were described from Portuguese estuaries, mainly from infections in the marine oligochaetes Limnodriloides agnes Hrabě, 1967 (Oligochaeta, Naididae), Tubificoides pseudogaster (Dahl, 1960) (Oligochaeta, Naididae) and Tubificoides insularis (Stephenson, 1923) (Rangel et al ., 2016 b ; Rocha et al ., 2019 c , 2020). Four types were reported to occur in freshwater, infecting Psammoryctides barbatus (Grube, 1861) (Oligochaeta, Naididae), and an unidentified species of the genus Potamothrix Vejdovský and Mrázek, 1903 (Oligochaeta, Naididae); this included one type that was also molecularly shown to occur in the marine oligochaete T. pseudogaster (Rocha et al ., 2020). The broader environmental range of this type was proposed to correlate with the biological features of the vertebrate host, namely its migratory patterns (Rocha et al ., 2020).…”

“…Four types were reported to occur in freshwater, infecting Psammoryctides barbatus (Grube, 1861) (Oligochaeta, Naididae), and an unidentified species of the genus Potamothrix Vejdovský and Mrázek, 1903 (Oligochaeta, Naididae); this included one type that was also molecularly shown to occur in the marine oligochaete T. pseudogaster (Rocha et al ., 2020). The broader environmental range of this type was proposed to correlate with the biological features of the vertebrate host, namely its migratory patterns (Rocha et al ., 2020).…”