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Abstract The early evolution of eukaryotes and their adaptations to low-oxygen environments are fascinating open questions in biology. Genome-scale data from novel eukaryotes, and particularly from free-living lineages, are the key to answering these questions. The Parabasalia are a major group of anaerobic eukaryotes that form the most speciose lineage of Metamonada. The most well-studied are parasitic parabasalids, including Trichomonas vaginalis and Tritrichomonas foetus, but very little genome-scale data are available for free-living members of the group. Here, we sequenced the transcriptome of Pseudotrichomonas keilini, a free-living parabasalian. Comparative genomic analysis indicated that P. keilini possesses a metabolism and gene complement that are in many respects similar to its parasitic relative T. vaginalis and that in the time since their most recent common ancestor, it is the T. vaginalis lineage that has experienced more genomic change, likely due to the transition to a parasitic lifestyle. Features shared between P. keilini and T. vaginalis include a hydrogenosome (anaerobic mitochondrial homolog) that we predict to function much as in T. vaginalis and a complete glycolytic pathway that is likely to represent one of the primary means by which P. keilini obtains ATP. Phylogenomic analysis indicates that P. keilini branches within a clade of endobiotic parabasalids, consistent with the hypothesis that different parabasalid lineages evolved toward parasitic or free-living lifestyles from an endobiotic, anaerobic, or microaerophilic common ancestor. 

ABSTRACT Human infections with the protozoanLophomonashave been increasingly reported in the medical literature over the past three decades. Initial reports were based on microscopic identification of the purported pathogen in respiratory specimens. Later, a polymerase chain reaction (PCR) was developed to detectLophomonas blattarum, following which there has been a significant increase in reports. In this minireview, we thoroughly examine the published reports ofLophomonasinfection to evaluate its potential role as a human pathogen. We examined the published images and videos of purportedLophomonas,compared its morphology and motility characteristics with host bronchial ciliated epithelial cells and trueL. blattarumderived from cockroaches, analyzed the published PCR that is being used for its diagnosis, and reviewed the clinical data of patients reported in the English and Chinese literature. From our analysis, we conclude that the images and videos from human specimens do not represent trueLophomonasand are predominantly misidentified ciliated epithelial cells. Additionally, we note that there is insufficient clinical evidence to attribute the cases toLophomonasinfection, as the clinical manifestations are non-specific, possibly caused by other infections and comorbidities, and there is no associated tissue pathology attributable toLophomonas. Finally, our analysis reveals that the published PCR is not specific toLophomonasand can amplify DNA from commensal trichomonads. Based on this thorough review, we emphasize the need for rigorous scientific scrutiny before a microorganism is acknowledged as a novel human pathogen and discuss the potential harms of misdiagnoses for patient care and scientific literature. 

ABSTRACT The symbiosis between termites and their hindgut protists is mutually obligate and vertically inherited. It was established by the late Jurassic in the cockroach ancestors of termites as they transitioned to wood feeding. Since then, protist symbionts have been transmitted from host generation to host generation by proctodeal trophallaxis (anal feeding). The protists belong to multiple lineages within the eukaryotic superphylum Metamonada. Most of these lineages have evolved large cells with complex morphology, unlike the non‐termite‐associated Metamonada. The species richness and taxonomic composition of symbiotic protist communities varies widely across termite lineages, especially within the deep‐branching clade Teletisoptera. In general, closely related termites tend to harbour closely related protists, and deep‐branching termites tend to harbour deep‐branching protists, reflecting their broad‐scale co‐diversification. A closer view, however, reveals a complex distribution of protist lineages across hosts. Some protist taxa are common, some are rare, some are widespread, and some are restricted to a single host family or genus. Some protist taxa can be found in only a few, distantly related, host species. Thus, the long history of co‐diversification in this symbiosis has been complicated by lineage‐specific loss of symbionts, transfer of symbionts from one host lineage to another, and by independent diversification of the symbionts relative to their hosts. This review aims to introduce the biology of this important symbiosis and serve as a gateway to the diversity and systematics literature for both termites and protists. A searchable database with all termite‐protist occurrence records and taxonomic references is provided as a supplementary file to encourage and facilitate new research in this field. 

Abstract Lophomonas blattarumis a facultative commensal gut dweller of common pest cockroaches. Its cells are roughly spherical in shape with an apical tuft of ~50 flagella. Controversially, it has been implicated in human respiratory infections based on light microscopic observations of similarly shaped cells in sputum or bronchoalveolar lavage fluid. Here, we have sequenced the 18S rRNA gene ofL. blattarumand its sole congener,Lophomonas striata, isolated from cockroaches. Both species branch in a fully supported clade with Trichonymphida, consistent with a previous study ofL. striata, but not consistent with sequences from human samples attributed toL. blattarum. 

Abstract Spirotrichonymphea, one of the six classes of phylum Parabasalia, are characterized by bearing many flagella in spiral rows, and they occur exclusively in the guts of termites. Phylogenetic relationships among the 13 described genera are not well understood due to complex morphological evolution and a paucity of molecular data. One such understudied genus isSpironympha. It has been variously considered a valid genus, a subgenus ofSpirotrichonympha, or an “immature” life cycle stage ofSpirotrichonympha. To clarify this, we sequenced the small subunit rRNA gene sequences ofSpironymphaandSpirotrichonymphacells isolated from the hindguts ofReticulitermesspecies andHodotermopsis sjostedtiand confirmed the molecular identity ofH. sjostedtisymbionts using fluorescence in situ hybridization.Spironymphaas currently circumscribed is polyphyletic, with bothH. sjostedtisymbiont species branching separately from the “true”SpironymphafromReticulitermes. Similarly, theSpirotrichonymphasymbiont ofH. sjostedtibranches separately from the “true”Spirotrichonymphafound inReticulitermes. Our data supportSpironymphafromReticulitermesas a valid genus most closely related toSpirotrichonympha, though its monophyly and interspecific relationships are not resolved in our molecular phylogenetic analysis. We propose three new genera to accommodate theH. sjostedtisymbionts and two new species ofSpirotrichonymphafromReticulitermes. 

This commentary paper addresses the outdated and misleading terminology used to categorize termites into “higher” and “lower”. These terms perpetuate a linear progression view of evolution, which is both inaccurate and detrimental to our understanding of the diversity of life. We trace the historical origins of these terms and highlight their flawed interpretation of evolutionary relationships. We advocate for the adoption of Termitidae (or termitid), rather than “higher termites”. As for the paraphyletic group of “lower termites”, we recommend refraining from grouping them together, unless specifically referring to their symbionts. In such cases, we propose “protist-dependent termites” or “non-Termitidae termites”. 

Many host-symbiont relationships are maintained through vertical transmission. While maternal symbiont transmission is common, biparental transmission is relatively rare. Protist-dependent termites are eusocial insects that harbor obligate, cellulolytic protists in their hindguts. Protists are vertically transmitted by winged reproductives (alates), which disperse to biparentally establish new colonies. Vertical transmission in protist-dependent termites is imperfect, as the protist communities of alates are often incomplete. Biparental transmission of protists may make it unnecessary for alates to harbor complete communities, as colonies would acquire symbionts from both founding kings and queens, which together may harbor sufficient inoculums. To investigate this hypothesis, the protist communities of Coptotermes gestroi and C. formosanus alates and colonies were examined using 18S rRNA amplicon sequencing. The complete protist communities of these Coptotermes species are composed of five parabasalid species each. Whereas alates often harbored 1–3 protist species, nearly all colonies harbored 4–5 species, implying biparental transmission. The probability of each protist species being present in at least one founding alate was used to determine expected protist occurrence in colonies. For most protists, expected and observed occurrence did not significantly differ, suggesting that each protist species only needs to be harbored by one founding alate to be acquired by colonies. Our results imply that biparental transmission allows founding reproductives to transmit adequate symbiont communities to colonies despite their individual communities being incomplete. We discuss biparental transmission in protist-dependent termites in the context of other biparentally transmitted symbioses.