Molecular phylogeny and ultrastructure of Selenidium serpulae (Apicomplexa, Archigregarinia) from the calcareous tubeworm Serpula vermicularis (Annelida, Polychaeta, Sabellida)

Abstract

213 Leander, B. S. (2007). Molecular phylogeny and ultrastructure of Selenidium serpulae (Apicomplexa, Archigregarinia) from the calcareous tubeworm Serpula vermicularis (Annelida, Polychaeta, Sabellida). 36 ,[213][214][215][216][217][218][219][220][221][222][223][224][225][226][227] Archigregarines are dynamic single-celled parasites that inhabit the intestinal systems of marine invertebrates, especially suspension feeding and deposit feeding polychaetes. Certain archigregarines in the genus Selenidium have retained several plesiomorphic characters, and improved knowledge of these species is expected to shed considerable light onto the earliest stages in apicomplexan evolution. Although archigregarines are related to some of the most notorious parasites known (e.g., C ryptosporidium and Plasmodium ), current knowledge of the group is meagre. In an attempt to improve our understanding of archigregarine diversity and evolution, I have characterised the general ultrastructure and molecular phylogenetic position of Selenidium serpulae (Lankester) Caullery and Mesnil. The parasites were isolated from the intestines of the calcareous tubeworm Serpula vermicularis (Polychaeta) collected in the eastern Pacific Ocean. The trophozoites (extracellular feeding stages) were spindle-shaped and capable of slow and continuous bending, and coiling, especially when dislodged from the host epithelium. The trophozoite surface was composed of 19 -23 longitudinal folds, prominent transverse folds and a robust, trilayered pellicle subtended by a single row of microtubules, each surrounded by an electron transparent sheath. Putative mitochondria were observed, but they were inconspicuous and apparently highly reduced, a condition that is indicative of anaerobic metabolism. The small subunit (SSU) rDNA sequence from S. serpulae was very closely related to two (short) sequences derived from an environmental PCR survey of an oxygendepleted hydrothermal vent system in the Gulf of California, namely C1-E017 (AY046619) and C2-E016 (AY046806). This result suggested that archigregarines with a morphology and lifecycle much like that in S. serpulae are thriving in this oxygen poor ecosystem. In addition, phylogenetic analyses of a larger SSU rDNA dataset (excluding the shorter environmental sequences) indicated that the nearest sister lineage to S. serpulae was S. vivax , a bizarre tape-like gregarine found in the intestines of sipunculids. This relationship was bolstered by comparative ultrastructural data and helped to illustrate that the diversification and biogeographical distribution of archigregarine parasites is probably more extensive than usually assumed.

Molecular Phylogeny of Marine Gregarine Parasites (Apicomplexa) from Tube‐forming Polychaetes (Sabellariidae, Cirratulidae, and Serpulidae), Including Descriptions of Two New Species of Selenidium

“…It is worthwhile to note here that an article published this year (Clopton ) argued strongly against the predominant use of molecular phylogenetic data for describing gregarine species, and perhaps organisms in general, in favor of a set of ideological rules based on detailed analyses of morphometric data; the promotion of these rules is intended to govern the way new species of gregarines should be described in the future. As reflected in our previous studies (Landers and Leander ; Leander ; Leander et al. ; Rueckert and Leander ; Rueckert et al.…”

“…This concept promotes the inference that Selenidium species have retained several morphological, ecological, and life history traits from distant ancestors that provide compelling insights into the earliest stages of apicomplexan evolution (Barta and Thompson ; Cox ; Dyson et al. ; Leander , ; Leander and Keeling ). Therefore, continued exploration of Selenidium diversity is expected to shed considerable light onto the deepest relationships within the phylogeny of apicomplexans and onto patterns of co‐evolution between gregarine apicomplexans and marine metazoan hosts (Leander ; Rueckert and Leander ; Théodoridès ).…”

“…Small subunit (SSU) rDNA sequences, for instance, are currently available from only seven of the approximately 60 described species of Selenidium , and it is expected that the vast majority of Selenidium species have yet to be discovered and characterized. As such, the phylogenetic relationships between Selenidium species and other lineages of marine gregarines remain unclear (Leander , ; Leander et al. ; Rueckert and Leander ; Wakeman and Leander ).…”

Motility in blastogregarines (Apicomplexa): Native and drug-induced organisation of Siedleckia nematoides cytoskeletal elements

“…It has been proposed that together they represent a unicellular analogue to the musculocuticular system of nematodes, in which longitudinal muscles function antagonistically against an elastic cuticle [41, 58]. Despite the striking similarity in motility mode and mechanism with Selenidium , however, the surface of S .…”

Molecular Phylogeny and Ultrastructure of Caliculium glossobalani n. gen. et sp. (Apicomplexa) from a Pacific Glossobalanus minutus (Hemichordata) Confounds the Relationships Between Marine and Terrestrial Gregarines

“…Molecular phylogenetic analyses of small subunit (SSU) rDNA sequences have reinforced this view by showing that species of archigregarines tend to have relatively short branches and represent five different lineages along the unresolved backbone of the apicomplexan tree; one of which, Veloxidium , forms the sister lineage to a diverse clade of marine lecudinids (Wakeman and Leander ). These results provide a compelling example for how the use of molecular phylogenetic approaches and increased sampling of new species have improved our understanding of gregarine diversity and evolutionary history (Leander , ; Rueckert and Leander ; Wakeman and Leander , ).…”