Marine gregarine genomes reveal the breadth of apicomplexan diversity with a partially conserved glideosome machinery

Abstract

Our current view of the evolutionary history, coding and adaptive capacities of Apicomplexa, protozoan parasites of a wide range of metazoan, is currently strongly biased toward species infecting humans, as data on early diverging apicomplexan lineages infecting invertebrates is extremely limited. Here, we characterized the genome of the marine eugregarine Porospora gigantea, intestinal parasite of Lobsters, remarkable for the macroscopic size of its vegetative feeding forms (trophozoites) and its gliding speed, the fastest so far recorded for Apicomplexa. Two highly syntenic genomes named A and B were assembled. Similar in size (~ 9 Mb) and coding capacity (~ 5300 genes), A and B genomes are 10.8% divergent at the nucleotide level, corresponding to 16–38 My in divergent time. Orthogroup analysis across 25 (proto)Apicomplexa species, including Gregarina niphandrodes, showed that A and B are highly divergent from all other known apicomplexan species, revealing an unexpected breadth of diversity. Phylogenetically these two species branch sisters to Cephaloidophoroidea, and thus expand the known crustacean gregarine superfamily. The genomes were mined for genes encoding proteins necessary for gliding, a key feature of apicomplexans parasites, currently studied through the molecular model called glideosome. Sequence analysis shows that actin-related proteins and regulatory factors are strongly conserved within apicomplexans. In contrast, the predicted protein sequences of core glideosome proteins and adhesion proteins are highly variable among apicomplexan lineages, especially in gregarines. These results confirm the importance of studying gregarines to widen our biological and evolutionary view of apicomplexan species diversity, and to deepen our understanding of the molecular bases of key functions such as gliding, well known to allow access to the intracellular parasitic lifestyle in Apicomplexa.

Identification of a new gregarine parasite associated with mass mortality events of freshwater pearl mussels (Margaritifera margaritifera) in Sweden

“…However, the assignment of this parasite to Nematopsis and its phylogenetic placement in a terrestrial clade challenged previous taxonomy based on morphology, which has considered Nematopsis as part of the marine clade Porosporidae (Cavalier-Smith, 2014;Rueckert et al, 2011). This is further conflicting with a recent study placing Porosporida gigantea as a sister group to marine gregarine and not with N. temporariae (Boisard et al, 2022). Thus, it is currently uncertain whether N. temporariae and the new associated diversity we describe here are truly members of the genus Nematopsis.…”

“…This is further conflicting with a recent study placing Porosporida gigantea as a sister group to marine gregarine and not with N . temporariae (Boisard et al., 2022). Thus, it is currently uncertain whether N .…”

Microscopic marine invertebrates are reservoirs for cryptic and diverse protists and fungi

“…It should be noted that short regions of the 18S SSU gene alone limit our ability to distinguish unique species; even distinct protistan species can have almost identical 18S genes [101]. Utilizing the full length of the 18S gene sequence would be the next step in improving the taxonomic resolution of our potential symbionts [102].…”

Genome sequence of Ophryocystis elektroscirrha, an apicomplexan parasite of monarch butterflies: cryptic diversity and response to host-sequestered plant chemicals

“…Prior to uploading, we trimmed the assemblies to remove contigs totaling fewer than 2,500 bases in length, both to meet requirements of the pipeline and because these contigs were unlikely to contain complete gene sequences. This approach resembles a recently successful effort to characterize the apicomplexan Porospora gigantea [ 5 ]. We then soft-masked the trimmed assembly after two independent rounds of repeat annotation, first with RepeatMasker v4.1.1 and then with RepeatModeler v2.0.1 before combining the two to mask bases for downstream analysis.…”

“…, and toxoplasmosis, from infections with Toxoplasma gondii [ 3 ]. Genomic studies of Apicomplexa have sequenced genomes that range from roughly 130 million bases on the high end [ 4 ] to a mere 9 million bases [ 5 ]; in other words, all Apicomplexa have small genomes compared to metazoans, but their genome sizes vary by an order of magnitude at least. Similarly, the gene content in these genomes is highly variable, from roughly 9,000 genes in T. gondii [ 6 ] to only 4,000 in the bovine parasite Theileria orientalis [ 7 ], a more than two-fold difference in gene content.…”