Evolutionary Origin and Host Range of Plagiotoma lumbrici (Ciliophora, Hypotrichia), an Obligate Gut Symbiont of Lumbricid Earthworms

Abstract

Four common earthworm species, the anecic Lumbricus terrestris, the endogeic Octolasion tyrteum as well as the epigeic Eisenia fetida and Dendrobaena veneta, were examined for the presence of the microbial gut symbiont Plagiotoma lumbrici. The evolutionary origin of this endobiotic microbe was reconstructed, using the 18S rRNA gene, the ITS1‐5.8S‐ITS2 region, and the first two domains of the 28S rRNA gene. Plagiotoma lumbrici was exclusively detected in the anecic Lumbricus terrestris. Multigene analyses and the ITS2 secondary structure robustly determined the phylogenetic home of Plagiotoma lumbrici populations within the oxytrichid Dorsomarginalia (Spirotrichea: Hypotrichia) as a sister taxon of the free‐living Hemiurosomoida longa. This indicates that earthworms obtained their gut endosymbiont by ingesting soil/leaf litter containing oxytrichine ciliates that became adapted to the intestinal tract of earthworms. Interestingly, according to the literature data, Plagiotoma lumbrici was detected in multiple anecic and some epigeic but never in endogeic earthworms. These observations suggest that Plagiotoma lumbrici might be adapted to certain gut conditions and the lifestyle of anecic Lumbricidae, such as Lumbricus, Aporrectodea, and Scherotheca, as well as of some co‐occurring epigeic Lumbricus species.

Concatenated data and dense taxon sampling clarify phylogeny and ecological transitions within Hypotricha

“…The analyses also reveal several marine-freshwater/ soil-marine transitions (Figures 1-4). And P. lumbricid, endobiotic ciliates in the gut endosymbiont of metazoan, falls into the clade with some oxytrichid species from freshwater (Figures 1-4), validating the hypothesis that this endobiotic species was descended from ingesting oxytrichine ciliates inhabited in soil by earthworms (Obert & Vd'ačný, 2020). Notably, many inferred transitions within Hypotricha depend upon genes and methods (Figures 1-4).…”

Diversity and Eco-Evolutionary Associations of Endosymbiotic Astome Ciliates With Their Lumbricid Earthworm Hosts

“…Therefore, Jankowski (2007, p. 901), referring to Aescht's Catalog, fixed "O. lumbrici Schrank, 1803" as type species of Anoplophrya. Jankowski (2007), however, overlooked that already de Puytorac (1954, p. 202) (Affa'a et al, 2004;Obert and Vd'ačný, 2020b). As concerns the three originally included species in Anoplophrya, only O. lumbrici Stein, 1854, remained classified in that genus after the revision of Heidenreich (1935).…”

Multi-Gene Phylogeny of the Ciliate Genus Trachelostyla (Ciliophora, Hypotrichia), With Integrative Description of Two Species, Trachelostyla multinucleata Spec. nov. and T. pediculiformis (Cohn, 1866)

“…More importantly, Caudikeronopsis and trachelostylids share multiple unique deletions in the ITS2 molecule, which caused their helix B to be composed of only one furcation loop and four subhelices (Figures 10, 11A,B,D). By contrast, helix B contains two furcation loops and five subhelices in all other hypotrichs (Figure 11D) and oligotrichs studied so far (e.g., Coleman, 2005;Weisse et al, 2008;Li et al, 2013;Zhan et al, 2019;Obert and Vd'ačný, 2020). The single furcation loop of Caudikeronopsis and trachelostylids corresponds to the second furcation loop of oligotrichs and other hypotrichs (Figure 11D).…”

“…Boundaries of ITS2 were determined according to Weisse et al (2008) as well as Obert and Vd’ačný (2020) . More specifically, we aligned trachelostylid sequences against Meseres corlissi (EU399522--29) and Plagiotoma lumbrici (MN176618--23), and then searched for the 5.8S-28S rRNA proximal stem of the ITS2 molecule.…”

“…The first furcation loop was apparently lost due to the complete deletion of subhelix B-5 already in the last common ancestor of Caudikeronopsis and trachelostylids. This loss also caused subhelices B-1 and B-2 to appear confluent in Caudikeronopsis and trachelostylids, whereas both subhelices are well recognizable in oligotrichs and all other hypotrichs (e.g., Coleman, 2005;Weisse et al, 2008;Li et al, 2013;Zhan et al, 2019;Obert and Vd'ačný, 2020).…”