Nephromyces, a beneficial apicomplexan symbiont in marine animals

Abstract

With malaria parasites (Plasmodium spp.), Toxoplasma, and many other species of medical and veterinary importance its iconic representatives, the protistan phylum Apicomplexa has long been defined as a group composed entirely of parasites and pathogens. We present here a report of a beneficial apicomplexan: the mutualistic marine endosymbiont Nephromyces. For more than a century, the peculiar structural and developmental features of Nephromyces, and its unusual habitat, have thwarted characterization of the phylogenetic affinities of this eukaryotic microbe. Using short-subunit ribosomal DNA (SSU rDNA) sequences as key evidence, with sequence identity confirmed by fluorescence in situ hybridization (FISH), we show that Nephromyces, originally classified as a chytrid fungus, is actually an apicomplexan. Inferences from rDNA data are further supported by the several apicomplexan-like structural features in Nephromyces, including especially the strong resemblance of Nephromyces infective stages to apicomplexan sporozoites. The striking emergence of the mutualistic Nephromyces from a quintessentially parasitic clade accentuates the promise of this organism, and the three-partner symbiosis of which it is a part, as a model for probing the factors underlying the evolution of mutualism, pathogenicity, and infectious disease.symbiosis | mutualism | parasitism | protist phylogeny | molgulid tunicate

Highly Dynamic Cellular-Level Response of Symbiotic Coral to a Sudden Increase in Environmental Nitrogen

“…The formation and further remobilization of uric acid crystals are also reported (i) in other endosymbiotic associations involving marine animal hosts, such as in the tripartite endosymbiosis between the tunicate Molgula manhattensis , its apicomplexan Nephromyces protist (phylogenetically related to the dinoflagellates, in the Alveolates supertaxon), and their symbiotic intracellular bacteria (40–42), and (ii) in the endosymbiosis between the acoel flatworm Symsagittifera roscoffensis and the green microalgae Tetraselmis convolutae (43). However, in these associations, unlike with our results with symbiotic corals, it is the host partner that produces uric acid deposits as transitory N stores, which are later remobilized through the uricolytic activity of their endosymbionts.…”

Evolution and genetic diversity of Theileria

“…This assumption rules out ticks as the initial hosts in which the early evolution of the piroplasmids might have occurred (Allsopp et al, 1994;Criado-Fornelio et al, 2003). Additionally, it is noteworthy that Nephromyces parasites of Molgula species (sea grapes) and Cardiosporidium cionae of ascidian Ciona intestinalis, which share a common ancestor with the piroplasmids, are not known to be vector transmitted (Ciancio et al, 2008;Saffo et al, 2010). If the piroplasmids initially evolved in vertebrate hosts, the next question is obvious: how did the ancestral piroplasmids complete their lifecycles?…”

Relationships Between Aquatic Protists and Humans

“…Endosymbiotic protists in digestive organs of termites and ruminants function in decomposition of plants, and are indirectly related to circulations of matters and energies, although such mutualistic protists seem to be rarely known in the aquatic ecosystems. An exception is a highly derived apicomplexan Nephromyces found in the renal sac of phylogenetically advanced molgulid tunicates, in which metabolic mutual aids between the apicomplexan, its symbiotic bacteria and the host are supposed (Saffo et al 2010 ). Ciliates and heterotrophic fl agellates function as consumers and decomposers in microbial loops and interstices, which are regarded as natural purifying facilities.…”