Ultrastructure and Molecular Phylogeny of Iotanema spirale gen. nov. et sp. nov., a New Lineage of Endobiotic Fornicata with Strikingly Simplified Ultrastructure

Abstract

Fornicata (Metamonada) is a group of Excavata living in low-oxygen environments and lacking conventional mitochondria. It includes free-living Carpediemonas-like organisms from marine habitats and predominantly parasitic/commensal retortamonads and diplomonads. Current modest knowledge of biodiversity of Fornicata limits our ability to draw a complete picture of the evolutionary history in this group. Here, we report the discovery of a novel fornicate, Iotanema spirale gen. nov. et sp. nov., obtained from fresh feces of the gecko Phelsuma madagascariensis. Our phylogenetic analyses of the small subunit ribosomal RNA gene demonstrate that I. spirale is closely related to the free-living, marine strain PCS and the Carpediemonas-like organism Hicanonectes teleskopos within Fornicata. Iotanema spirale exhibits several features uncommon to fornicates, such as a single flagellum, a highly reduced cytoskeletal system, and the lack of the excavate ventral groove, but shares these characters with the poorly known genus Caviomonas. Therefore, I. spirale is accommodated within the family Caviomonadidae, which represents the third known endobiotic lineage of Fornicata. This study improves our understanding of character evolution within Fornicata when placed within the molecular phylogenetic context.

Retortamonads from vertebrate hosts share features of anaerobic metabolism and pre-adaptations to parasitism with diplomonads

“…4 ) and thus represents a conserved biological process to survive adverse conditions and spread among hosts. Surprisingly, cysts are infrequently observed among CLOs, so far documented in Hicanonectes telescopos and Iotanema spirale [ 37 , 38 ]. Another example of a biological process that is not directly obvious from ultrastructural observations is the presence of a Golgi apparatus.…”

Proposal for practical multi-kingdom classification of eukaryotes based on monophyly and comparable divergence time criteria

“…I compared the classifications against >200 phylogenetic studies from class to kingdom levels, giving priority to studies with larger ingroup, greater number of genes and most recent treatments (for minor deep diverging groups). In brief, the following studies were used to extract much of the class to domain level classification information: Yoon et al (2006), Ruhfel et al (2014), Magallon et al (2015), Leliaert et al (2017) (Archaeplastida); Fiore-Donno et al (2010), Lahr et al (2013), Cavalier-Smith et al (2015b, 2016), Tekle et al (2016), Kang et al (2017), Tekle & Wood 2017 (Amoebozoa); Kolisko 2011, Kamikawa et al (2014), Radek et al (2014), Cavalier-Smith (2016), Yubuki et al (2017) (Excavata); Grant et al (2009), Riisberg et al (2009), Brown & Sorhannus (2010), Yang et al (2012), Cavalier-Smith & Scoble (2013), Shiratori et al (2015, 2017), Yubuki et al (2015), Aleoshin et al (2016), Derelle et al (2016), Dumack (2016), Gao et al (2016), Krabberød et al 2017, Reñé et al (2017) (Harosa); Brown et al (2009, 2013), Cavalier-Smith & Chao (2010), Zhang (2011), Glücksman et al (2013), Nosenko et al 2013, Paps et al (2013), Yabuki et al (2013), Telford et al 2015; Torruella et al (2015), Whelan et al (2015), Corsaro et al (2016), Carr et al (2017), Dohrmann & Wöhrheide (2017), Hehenberger et al (2017), Schiffer et al (2017), Simion et al (2017), Tedersoo et al (2018), (Opisthokonta); Yoon et al (2008, 2011), Wegener Parfrey et al (2010, 2011), Burki et al (2012, 2016), Cavalier-Smith & Chao (2012), Yabuki et al (2012, 2014) Cavalier-Smith et al (2014, 2015a), Burki (2014), Katz & Grant (2014), Sharpe et al (2015), Brown et al (2017) (minor groups and all eukaryotes). Following the divergence time estimates of Wegener Parfrey et al (2011),...…”

Evidence for an Independent Hydrogenosome-to-Mitosome Transition in the CL3 Lineage of Fornicates

“…The single transmission electron microscopy (TEM) study of this organism did not reveal any candidate for a mitochondrion or a MRO ( Brugerolle and Regnault, 2001 ). The phylogenetic position of C. mobilis had remained uncertain due to a lack of molecular data, but recently a putative specific relative sharing important morphological and ultrastructural features was isolated from gecko feces and described as Iotanema spirale ( Yubuki et al, 2017 ). Phylogenetic analyses based on 18S rRNA gene sequences placed I. spirale into Fornicata, specifically into the informal CL3 clade previously established for two free-living marine flagellates Hicanonectes teleskopos and a formally undescribed isolate, PCS ( Kolisko et al, 2010 ).…”

“…Phylogenetic analyses based on 18S rRNA gene sequences placed I. spirale into Fornicata, specifically into the informal CL3 clade previously established for two free-living marine flagellates Hicanonectes teleskopos and a formally undescribed isolate, PCS ( Kolisko et al, 2010 ). Within the CL3 group, I. spirale , and presumably also Caviomonas spp., are specifically related to the PCS strain ( Yubuki et al, 2017 ). Since Caviomonas , Iotanema , and PCS are similar in gross morphology, the latter is considered a member of Caviomonadidae ( Yubuki et al, 2017 ).…”

“…Within the CL3 group, I. spirale , and presumably also Caviomonas spp., are specifically related to the PCS strain ( Yubuki et al, 2017 ). Since Caviomonas , Iotanema , and PCS are similar in gross morphology, the latter is considered a member of Caviomonadidae ( Yubuki et al, 2017 ). No mitochondrion or MRO candidate was discerned in I. spirale by TEM ( Yubuki et al, 2017 ), which contrasts with the presence of a readily observable hydrogenosome-like organelle in H. teleskopos ( Park et al, 2009 ); no TEM data was available for PCS.…”