Taxonomic Resolution of Blood-Infecting Apicomplexans of Teleost Fish and Gnathiids: Ichthyocolida ord. nov.
Marine fish (teleosts) have historically been shown to be infected with blood-borne apicomplexans, with gnathiids serving as a likely vector. For over a century, these parasites have been morphologically characterized as hemogregarines within the suborder Adeleorina of Apicomplexa. Molecular studies in recent years have suggested that these parasites may actually be more closely related to coccidians, specifically as sister to the coral-infecting corallicolids. Recent phylogenetic analyses of Haemogregarina bigemina from Ophioblennius macclurei confirmed these findings and identified these parasites as widespread across marine fish diversity and marine habitats. Although informally referred to as ichthyocolids, these parasites remain formally undescribed, hindering the development of a cohesive taxonomic framework for their continued study. To address this, we performed metatranscriptomic sequencing of infected longfin damselfish (Stegastes diencaeus) blood for phylogenomic analysis. By combining these data with those from infected O. macclurei blood, we expanded genomic sampling for this lineage and formally describe this group taxonomically. Phylogenomic analysis incorporating 164 conserved nuclear genes confirms this clade as sister to Corallicolida, with the combined clade closely related to Protococcidia. 18S-28S rRNA gene phylogenetics reveal extensive diversity within the ichthyocolids and a degree of host specificity. From these results, we formally assign this clade of fish apicomplexan parasites to a new order, Ichthyocolida ord. nov., and family, Ichthyocolidae fam. nov. To avoid confusion with true hemogregarines, we reassign H. bigemina from O. macclurei to Ichthyocola bigemina comb. nov. We also describe a new genus of damselfish-associated ichthyocolids, Pomacentriphila gen. nov., including the species P. dushii from S. diencaeus in the southern Caribbean. We hope that this taxonomic framework will enable further study of these parasites given their cosmopolitan distribution and interesting evolutionary history.