Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles

Abstract

The phylum Apicomplexa comprises human pathogens such as Plasmodium but is also an under-explored hotspot of evolutionary diversity central to understanding the origins of parasitism and non-photosynthetic plastids. We generated single-cell transcriptomes for all major apicomplexan groups lacking large-scale sequence data. Phylogenetic analysis reveals that apicomplexan-like parasites are polyphyletic and their similar morphologies emerged convergently at least three times. Gregarines and eugregarines are monophyletic, against most expectations, and rhytidocystids and Eleutheroschizon are sister lineages to medically important taxa. Although previously unrecognized, plastids in deep-branching apicomplexans are common, and they contain some of the most divergent and AT-rich genomes ever found. In eugregarines, however, plastids are either abnormally reduced or absent, thus increasing known plastid losses in eukaryotes from two to four. Environmental sequences of ten novel plastid lineages and structural innovations in plastid proteins confirm that plastids in apicomplexans and their relatives are widespread and share a common, photosynthetic origin.

Why the –omic future of Apicomplexa should include gregarines

“…Indeed, the genomic knowledge on apicomplexan is currently highly biased in favour of intracellular parasites of vertebrate hosts, belonging to Haematozoa, Coccidia and to a lesser extent, Cryptosporidia (Figure 1). Gregarines have been so far mostly excluded from this –omic exploration, to the exception of (unpublished) genome of the terrestrial insect eugregarine Gregarina niphandrodes (accessible at EupathDB (Aurrecoechea et al., 2017), section CryptoDB), intestinal parasite of Tenebrio molitor , very partial genomic data on insect eugregarine Ascogregarina taiwanensis (Templeton et al., 2010) intestinal parasite of Aedes albopictus and partial and recently emerging transcriptomic data for a dozen of terrestrial and marine gregarine species (Omoto et al., 2004; Janouskovec et al., 2019; Mathur et al., 2019) (see Figure 1 for illustration on Apicomplexa genomic data knowledge).…”

“…Attempts to improve phylogenies using the full ribosomal marker (18S SSU + 28S LSU rDNA) have provided some progress, but have the important disadvantage to be currently available for only very few gregarine species (∼20) (Diakin et al., 2016; Diakin et al., 2017; Simdyanov et al., 2018). Phylogenies relying on multiple genes (or more accurately proteins) sequences derived from genome/transcriptome investigations are now emerging but remain restrained to a dozen of gregarine species (Janouskovec et al., 2019; Mathur et al., 2019). Although they are indeed expected to be more resolving, the number of concerned species is even smaller and ambiguities remain in the interrelationships between groups, since the position of the genus Cryptosporidium is for example unstable between the two studies (Janouskovec et al., 2019; Mathur et al., 2019).…”

“…Phylogenies relying on multiple genes (or more accurately proteins) sequences derived from genome/transcriptome investigations are now emerging but remain restrained to a dozen of gregarine species (Janouskovec et al., 2019; Mathur et al., 2019). Although they are indeed expected to be more resolving, the number of concerned species is even smaller and ambiguities remain in the interrelationships between groups, since the position of the genus Cryptosporidium is for example unstable between the two studies (Janouskovec et al., 2019; Mathur et al., 2019). These genome/transcriptome studies have however also shown another interest: some species historically described as gregarines ( Platyproteum sp.…”

“…These genome/transcriptome studies have however also shown another interest: some species historically described as gregarines ( Platyproteum sp. and Digyalum oweni ) do not actually appear anymore to be part of Apicomplexa (Janouskovec et al., 2019; Mathur et al., 2019).…”

“…Cryptosporidium, Eimeria ), other alternate between two successive hosts (dixenous parasites such as Plasmodium , Babesia and Theileria , completing sexual reproduction in various insects or arthropods and asexual phases in various tissues of vertebrates) and few have the capacity to infect multiple hosts (polyxenous parasites such as Toxoplasma , completing its sexual reproduction in cats and several asexual phases in various tissues of diverse warm blooded vertebrates). Due to their medical, veterinary or economical importance, and because it has been possible to cultivate most of them in laboratory conditions, their genomes have been deciphered (∼100, deposited into the EupathDB database (Aurrecoechea et al., 2017), Figure 1) and are major references for medical investigations, comparative genomics studies and exploration of evolutionary history of apicomplexan parasites (Janouskovec et al., 2015; Woo et al., 2015; Janouskovec et al., 2019; Kwong et al., 2019).…”