ABSTRACT
Human infections with the protozoan Lophomonas have 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 detect Lophomonas blattarum, following which there has been a significant increase in reports. In this minireview, we thoroughly examine the published reports of Lophomonas infection to evaluate its potential role as a human pathogen. We examined the published images and videos of purported Lophomonas, compared its morphology and motility characteristics with host bronchial ciliated epithelial cells and true L. blattarum derived 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 true Lophomonas and are predominantly misidentified ciliated epithelial cells. Additionally, we note that there is insufficient clinical evidence to attribute the cases to Lophomonas infection, as the clinical manifestations are non-specific, possibly caused by other infections and comorbidities, and there is no associated tissue pathology attributable to Lophomonas. Finally, our analysis reveals that the published PCR is not specific to Lophomonas and 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.
Subject(s)
Parabasalidea , Protozoan Infections , Humans , Protozoan Infections/diagnosis , Diagnostic ErrorsABSTRACT
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.
Subject(s)
Isoptera , Animals , Phylogeny , Eukaryota , SymbiosisABSTRACT
Lophomonas blattarum is 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 of L. blattarum and its sole congener, Lophomonas striata, isolated from cockroaches. Both species branch in a fully supported clade with Trichonymphida, consistent with a previous study of L. striata, but not consistent with sequences from human samples attributed to L. blattarum.
Subject(s)
Cockroaches , Parabasalidea , Animals , Humans , Parabasalidea/genetics , Phylogeny , RNA, Ribosomal, 18S/genetics , FlagellaABSTRACT
In the Samail Ophiolite of Oman, the geological process of serpentinization produces reduced, hydrogen rich, hyperalkaline (pH > 11) fluids. These fluids are generated through water reacting with ultramafic rock from the upper mantle in the subsurface. On Earth's continents, serpentinized fluids can be expressed at the surface where they can mix with circumneutral surface water and subsequently generate a pH gradient (â¼pH 8 to pH > 11) in addition to variations in other chemical parameters such as dissolved CO2, O2, and H2. Globally, archaeal and bacterial community diversity has been shown to reflect geochemical gradients established by the process of serpentinization. It is unknown if the same is true for microorganisms of the domain Eukarya (eukaryotes). In this study, using 18S rRNA gene amplicon sequencing, we explore the diversity of microbial eukaryotes called protists in sediments of serpentinized fluids in Oman. We demonstrate that protist community composition and diversity correlate significantly with variations in pH, with protist richness being significantly lower in sediments of hyperalkaline fluids. In addition to pH, the availability of CO2 to phototrophic protists, the composition of potential food sources (prokaryotes) for heterotrophic protists and the concentration of O2 for anaerobic protists are factors that likely shape overall protist community composition and diversity along the geochemical gradient. The taxonomy of the protist 18S rRNA gene sequences indicates the presence of protists that are involved in carbon cycling in serpentinized fluids of Oman. Therefore, as we evaluate the applicability of serpentinization for carbon sequestration, the presence and diversity of protists should be considered.
ABSTRACT
Hot spring outflow channels provide geochemical gradients that are reflected in microbial community compositions. In many hot spring outflows, there is a distinct visual demarcation as the community transitions from predominantly chemotrophs to having visible pigments from phototrophs. It has been hypothesized that this transition to phototrophy, known as the photosynthetic fringe, is a result of the pH, temperature, and/or sulfide concentration gradients in the hot spring outflows. Here, we explicitly evaluated the predictive capability of geochemistry in determining the location of the photosynthetic fringe in hot spring outflows. A total of 46 samples were taken from 12 hot spring outflows in Yellowstone National Park that spanned pH values from 1.9 to 9.0 and temperatures from 28.9 to 92.2°C. Sampling locations were selected to be equidistant in geochemical space above and below the photosynthetic fringe based on linear discriminant analysis. Although pH, temperature, and total sulfide concentrations have all previously been cited as determining factors for microbial community composition, total sulfide did not correlate with microbial community composition with statistical significance in non-metric multidimensional scaling. In contrast, pH, temperature, ammonia, dissolved organic carbon, dissolved inorganic carbon, and dissolved oxygen did correlate with the microbial community composition with statistical significance. Additionally, there was observed statistical significance between beta diversity and the relative position to the photosynthetic fringe with sites above the photosynthetic fringe being significantly different from those at or below the photosynthetic fringe according to canonical correspondence analysis. However, in combination, the geochemical parameters considered in this study only accounted for 35% of the variation in microbial community composition determined by redundancy analysis. In co-occurrence network analyses, each clique correlated with either pH and/or temperature, whereas sulfide concentrations only correlated with individual nodes. These results indicate that there is a complex interplay between geochemical variables and the position of the photosynthetic fringe that cannot be fully explained by statistical correlations with the individual geochemical variables included in this study.
ABSTRACT
The eukaryotic phylum Parabasalia is composed primarily of anaerobic, endobiotic organisms such as the veterinary parasite Tritrichomonas foetus and the human parasite Trichomonas vaginalis, the latter causing the most prevalent, non-viral, sexually transmitted disease world-wide. Although a parasitic lifestyle is generally associated with a reduction in cell biology, T. vaginalis provides a striking counter-example. The 2007 T. vaginalis genome paper reported a massive and selective expansion of encoded proteins involved in vesicle trafficking, particularly those implicated in the late secretory and endocytic systems. Chief amongst these were the hetero-tetrameric adaptor proteins or 'adaptins', with T. vaginalis encoding â¼3.5 times more such proteins than do humans. The provenance of such a complement, and how it relates to the transition from a free-living or endobiotic state to parasitism, remains unclear. In this study, we performed a comprehensive bioinformatic and molecular evolutionary investigation of the heterotetrameric cargo adaptor-derived coats, comparing the molecular complement and evolution of these proteins between T. vaginalis, T. foetus and the available diversity of endobiotic parabasalids. Notably, with the recent discovery of Anaeramoeba spp. as the free-living sister lineage to all parabasalids, we were able to delve back to time points earlier in the lineage's history than ever before. We found that, although T. vaginalis still encodes the most HTAC subunits amongst parabasalids, the duplications giving rise to the complement took place more deeply and at various stages across the lineage. While some duplications appear to have convergently shaped the parasitic lineages, the largest jump is in the transition from free-living to endobiotic lifestyle with both gains and losses shaping the encoded complement. This work details the evolution of a cellular system across an important lineage of parasites and provides insight into the evolutionary dynamics of an example of expansion of protein machinery, counter to the more common trends observed in many parasitic systems.
Subject(s)
Parabasalidea , Parasites , Trichomonas vaginalis , Tritrichomonas foetus , Animals , Humans , Trichomonas vaginalis/genetics , Tritrichomonas foetus/genetics , Computational BiologyABSTRACT
Mitochondria originated from an ancient bacterial endosymbiont that underwent reductive evolution by gene loss and endosymbiont gene transfer to the nuclear genome. The diversity of mitochondrial genomes published to date has revealed that gene loss and transfer processes are ongoing in many lineages. Most well-studied eukaryotic lineages are represented in mitochondrial genome databases, except for the superphylum Retaria-the lineage comprising Foraminifera and Radiolaria. Using single-cell approaches, we determined two complete mitochondrial genomes of Foraminifera and two nearly complete mitochondrial genomes of radiolarians. We report the complete coding content of an additional 14 foram species. We show that foraminiferan and radiolarian mitochondrial genomes contain a nearly fully overlapping but reduced mitochondrial gene complement compared to other sequenced rhizarians. In contrast to animals and fungi, many protists encode a diverse set of proteins on their mitochondrial genomes, including several ribosomal genes; however, some aerobic eukaryotic lineages (euglenids, myzozoans, and chlamydomonas-like algae) have reduced mitochondrial gene content and lack all ribosomal genes. Similar to these reduced outliers, we show that retarian mitochondrial genomes lack ribosomal protein and tRNA genes, contain truncated and divergent small and large rRNA genes, and contain only 14 or 15 protein-coding genes, including nad1, -3, -4, -4L, -5, and -7, cob, cox1, -2, and -3, and atp1, -6, and -9, with forams and radiolarians additionally carrying nad2 and nad6, respectively. In radiolarian mitogenomes, a noncanonical genetic code was identified in which all three stop codons encode amino acids. Collectively, these results add to our understanding of mitochondrial genome evolution and fill in one of the last major gaps in mitochondrial sequence databases. IMPORTANCE We present the reduced mitochondrial genomes of Retaria, the rhizarian lineage comprising the phyla Foraminifera and Radiolaria. By applying single-cell genomic approaches, we found that foraminiferan and radiolarian mitochondrial genomes contain an overlapping but reduced mitochondrial gene complement compared to other sequenced rhizarians. An alternative genetic code was identified in radiolarian mitogenomes in which all three stop codons encode amino acids. Collectively, these results shed light on the divergent nature of the mitochondrial genomes from an ecologically important group, warranting further questions into the biological underpinnings of gene content variability and genetic code variation between mitochondrial genomes.
Subject(s)
Foraminifera , Genome, Mitochondrial , Rhizaria , Animals , Foraminifera/genetics , Phylogeny , Codon, Terminator , Rhizaria/genetics , Genomics , Eukaryota/genetics , Amino Acids/genetics , DNA, Mitochondrial/geneticsABSTRACT
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 is Spironympha. It has been variously considered a valid genus, a subgenus of Spirotrichonympha, or an "immature" life cycle stage of Spirotrichonympha. To clarify this, we sequenced the small subunit rRNA gene sequences of Spironympha and Spirotrichonympha cells isolated from the hindguts of Reticulitermes species and Hodotermopsis sjostedti and confirmed the molecular identity of H. sjostedti symbionts using fluorescence in situ hybridization. Spironympha as currently circumscribed is polyphyletic, with both H. sjostedti symbiont species branching separately from the "true" Spironympha from Reticulitermes. Similarly, the Spirotrichonympha symbiont of H. sjostedti branches separately from the "true" Spirotrichonympha found in Reticulitermes. Our data support Spironympha from Reticulitermes as a valid genus most closely related to Spirotrichonympha, though its monophyly and interspecific relationships are not resolved in our molecular phylogenetic analysis. We propose three new genera to accommodate the H. sjostedti symbionts and two new species of Spirotrichonympha from Reticulitermes.
Subject(s)
Isoptera , Parabasalidea , Animals , Parabasalidea/genetics , Phylogeny , In Situ Hybridization, Fluorescence , Symbiosis , Digestive SystemABSTRACT
Microjoenia are obligate symbionts of termites. The genus was erected in 1892 for small cells with many flagella that insert near, but not directly from, the cell apex, and an axostyle that can protrude from the cell posterior. Although ultrastructural studies have been carried out on three Microjoenia species to date, no molecular data have been directly attributed to any species. Microjoenia are classified within the parabasalian class Spirotrichonymphea, which is characterized by flagellar bands that emerge near the cell apex and proceed posteriorly in a right-handed helix. In Microjoenia, however, the flagellar bands are very short and proceed longitudinally or with a weakly observable helix. In this study, we have amplified and sequenced the 18S ribosomal RNA gene from individually isolated Microjoenia cells from Reticulitermes and Hodotermopsis hosts as part of an ongoing effort to understand the phylogeny of Spirotrichonymphea and their coevolution with termites. In our 18S rRNA gene phylogeny, Microjoenia forms the sister lineage to Spirotrichonympha, though many other evolutionary relationships within Spirotrichonymphea remain unresolved.
Subject(s)
Isoptera , Parabasalidea , Animals , Parabasalidea/genetics , Phylogeny , RNA, Ribosomal, 18S/genetics , SymbiosisABSTRACT
Air carries a diverse load of particulate microscopic biological matter in suspension, either aerosolized or aggregated with dust particles, the aerobiome, which is dispersed by winds from sources to sinks. The aerobiome is known to contain microbes, including pathogens, as well as debris or small-sized propagules from plants and animals, but its variability and composition has not been studied comprehensibly. To gain a dynamic insight into the aerobiome existing over a mixed-use dryland setting, we conducted a biologically comprehensive, year-long survey of its composition and dynamics for particles less than 10 µm in diameter based on quantitative analyses of DNA content coupled to genomic sequencing. Airborne biological loads were more dependent on seasonal events than on meteorological conditions and only weakly correlated with dust loads. Core aerobiome species could be understood as a mixture of high elevation (e.g. Microbacteriaceae, Micrococcaceae, Deinococci), and local plant and soil sources (e.g. Sphingomonas, Streptomyces, Acinetobacter). Despite the mixed used of the land surrounding the sampling site, taxa that contributed to high load events were largely traceable to proximal agricultural practices like cotton and livestock farming. This included not only the predominance of specific crop plant signals over those of native vegetation, but also that of their pathogens (bacterial, viral and eukaryotic). Faecal bacterial loads were also seasonally important, possibly sourced in intensive animal husbandry or manure fertilization activity, and this microbial load was enriched in tetracycline resistance genes. The presence of the native opportunistic pathogen, Coccidioides spp., by contrast, was detected only with highly sensitive techniques, and only rarely. We conclude that agricultural activity exerts a much stronger influence that the native vegetation as a mass loss factor to the land system and as an input to dryland aerobiomes, including in the dispersal of plant, animal and human pathogens and their genetic resistance characteristics.
Subject(s)
Agriculture , Soil , Animals , Humans , Manure , Plants , SeasonsABSTRACT
The desert dampwood termite Paraneotermes simplicicornis harbors several species of obligately symbiotic protists that support its nutrition by fermenting lignocellulose. Among them are three morphotypes with the dexiotropic spiraling flagellar bands characteristic of Spirotrichonymphea (Parabasalia). The largest morphotype, characterized by an elongated cell apex with axial columella and internally positioned spiraling flagellar bands, was previously described as Spirotrichonympha polygyra. A smaller morphotype, with similarly internalized flagellar bands but a more rounded posterior without a protruding axostyle, was previously reported but not named. The smallest morphotype has surface flagellar bands and can attach to other protist cells by its apex. In this study, we combine light microscopy of live specimens and 18S rRNA gene sequencing of individually isolated cells to better understand the diversity of symbionts in P. simplicicornis. We found that S. polygyra branches distantly from true Spirotrichonympha, which are associated with Reticulitermes termites. Thus, we propose the new genus Cuppa to accommodate C. polygyra n. comb. (type species) and the similar but smaller morphotype Cuppa taenia n. sp. The undescribed smallest morphotype can be excluded from all previously described Spirotrichonymphea genera by molecular and behavioral evidence, so we propose Fraterculus simplicicornis n. gen., n. sp., to accommodate this organism.
Subject(s)
Isoptera/parasitology , Parabasalidea/classification , Parabasalidea/physiology , Symbiosis , Animals , DNA, Protozoan/genetics , Parabasalidea/genetics , Phylogeny , RNA, Ribosomal, 18S/genetics , Species SpecificityABSTRACT
Coptotermes formosanus Shiraki and Coptotermes gestroi (Wasmann) (Blattoidea: Rhinotermitidae) are invasive subterranean termite pest species with a major global economic impact. However, the descriptions of the mutualistic protist communities harbored in their respective hindguts remain fragmentary. The C. formosanus hindgut has long been considered to harbor three protist species, Pseudotrichonympha grassii (Trichonymphida), Holomastigotoides hartmanni, and Cononympha (Spirotrichonympha) leidyi (Spirotrichonymphida), but molecular data have suggested that the diversity may be higher. Meanwhile, the C. gestroi community remains undescribed except for Pseudotrichonympha leei. To complete the characterization of these communities, hindguts of workers from both termite species were investigated using single-cell PCR, microscopy, cell counts, and 18S rRNA amplicon sequencing. The two hosts were found to harbor intriguingly parallel protist communities, each consisting of one Pseudotrichonympha species, two Holomastigotoides species, and two Cononympha species. All protist species were unique to their respective hosts, which last shared a common ancestor ~18 MYA. The relative abundances of protist species in each hindgut differed remarkably between cell count data and 18S rRNA profiles, calling for caution in interpreting species abundances from amplicon data. This study will enable future research in C. formosanus and C. gestroi hybrids, which provide a unique opportunity to study protist community inheritance, compatibility, and potential contribution to hybrid vigor.
Subject(s)
Digestive System/parasitology , Isoptera/parasitology , Parabasalidea/classification , Parabasalidea/genetics , Animals , DNA, Protozoan/genetics , Host-Parasite Interactions , Phylogeny , Polymerase Chain Reaction , RNA, Ribosomal, 18S/genetics , Single-Cell Analysis , SymbiosisABSTRACT
Hoplonympha natator is an obligate symbiont of Paraneotermes simplicicornis (Kalotermitidae), from southwestern North America. Another Hoplonympha species inhabits Hodotermopsis sjostedti (Archotermopsidae), from montane Southeast Asia. The large phylogenetic and geographical distance between the hosts makes the distribution of Hoplonympha puzzling. Here, we report the phylogenetic position of H. natator from P. simplicicornis through maximum likelihood and Bayesian analysis of 18S rRNA genes. The two Hoplonympha species form a clade with a deep node, making a recent symbiont transfer unlikely. The distribution of Hoplonympha may be due to an ancient transfer or strict vertical inheritance with differential loss from other hosts.
Subject(s)
Isoptera/parasitology , Parabasalidea/classification , Animals , Arizona , Bayes Theorem , Parabasalidea/genetics , Phylogeny , RNA, Protozoan/analysis , RNA, Ribosomal, 18S/analysis , Species Specificity , SymbiosisABSTRACT
A central challenge in measuring the biophysical properties of cells with electrokinetic approaches is the assignment of these biophysical properties to specific biological characteristics. Changes in the electrokinetic behavior of cells may come from mutations, altered gene expression levels, post-translation modifications, or environmental effects. Here we assess the electrokinetic behavior of chemically surface-modified bacterial cells in order to gain insight into the biophysical properties that are specifically affected by changes in surface chemistry. Using E. coli as a scaffold, an amine coupling reaction was used to covalently attach glycine, spermine, bovine serum albumin (protein), or 7-amino-4-methyl-3-coumarinylacetic acid (fluorescent dye) to the free carboxylic acid groups on the surface of the cells. These populations, along with unlabeled control cells, were subject to electrokinetic and dielectrophoretic measurements to quantify any changes in the biophysical properties upon alteration. The properties associated with each electrokinetic force are discussed relative to the specific reactant used. We conclude that relatively modest and superficial changes to cell surfaces can cause measurable changes in their biophysical properties.
ABSTRACT
Termites have a unique ability to effectively digest lignocellulose with the help of mutualistic symbionts. While gut bacteria and protozoa have been relatively well characterized in termites, the virome remains largely unexplored. Here, we report two genomes of microviruses (termite-associated microvirus-1 [TaMV-1] and termite-associated microvirus-2 [TaMV-2]) associated with the gut of Coptotermes formosanus.
ABSTRACT
Holomastigotes is a protist genus (Parabasalia: Spirotrichonymphea) that resides in the hindguts of "lower" termites. It can be distinguished from other parabasalids by spiral flagellar bands that run along the entire length of the cell, an anterior nucleus, a reduced or absent axostyle, the presence of spherical vesicles inside the cells, and the absence of ingested wood particles. Eight species have been described based on their morphology so far, although no molecular data were available prior to this study. We determined the 18S rRNA gene sequences of Holomastigotes from the hindguts of Hodotermopsis sjostedti, Reticulitermes flavipes, Reticulitermes lucifugus, and Reticulitermes tibialis. Phylogenetic analyses placed all sequences in an exclusive and well-supported clade with the type species, Holomastigotes elongatum from R. lucifugus. However, the phylogenetic position of Holomastigotes within the Spirotrichonymphea was not resolved. We describe two new species, Holomastigotes flavipes n. sp. and Holomastigotes tibialis n. sp., inhabiting the hindguts of R. flavipes and R. tibialis, respectively.
Subject(s)
Isoptera/parasitology , Parabasalidea/classification , Animals , Digestive System/parasitology , Parabasalidea/cytology , Parabasalidea/genetics , Phylogeny , RNA, Protozoan/analysis , RNA, Ribosomal, 18S/analysis , SymbiosisABSTRACT
The division of life into producers and consumers is blurred by evolution. For example, eukaryotic phototrophs can lose the capacity to photosynthesize, although they may retain vestigial plastids that perform other essential cellular functions. Chrysophyte algae have undergone a particularly large number of photosynthesis losses. Here, we present a plastid genome sequence from a nonphotosynthetic chrysophyte, "Spumella" sp. NIES-1846, and show that it has retained a nearly identical set of plastid-encoded functions as apicomplexan parasites. Our transcriptomic analysis of 12 different photosynthetic and nonphotosynthetic chrysophyte lineages reveals remarkable convergence in the functions of these nonphotosynthetic plastids, along with informative lineage-specific retentions and losses. At one extreme, Cornospumella fuschlensis retains many photosynthesis-associated proteins, although it appears to have lost the reductive pentose phosphate pathway and most plastid amino acid metabolism pathways. At the other extreme, Paraphysomonas lacks plastid-targeted proteins associated with gene expression and all metabolic pathways that require plastid-encoded partners, indicating a complete loss of plastid DNA in this genus. Intriguingly, some of the nucleus-encoded proteins that once functioned in the expression of the Paraphysomonas plastid genome have been retained. These proteins were likely to have been dual targeted to the plastid and mitochondria of the chrysophyte ancestor, and are uniquely targeted to the mitochondria in Paraphysomonas Our comparative analyses provide insights into the process of functional reduction in nonphotosynthetic plastids.
Subject(s)
Chrysophyta/genetics , Evolution, Molecular , Genome, Plastid , Plastids/genetics , Chloroplast Proteins/genetics , Gene Expression Profiling , Gene Expression RegulationABSTRACT
Dinoflagellates are some of the most common eukaryotic cells in the ocean, but have very unusual nuclei. Many exhibit a form of closed mitosis (dinomitosis) wherein the nuclear envelope (NE) invaginates to form one or more trans-nuclear tunnels. Rather than contact spindles directly, the chromatids then bind to membrane-based kinetochores on the NE. To better understand these unique mitotic features, we reconstructed the nuclear architecture of Polykrikos kofoidii in 3D using focused ion beam scanning electron microscopy (FIB-SEM) in conjunction with high-pressure freezing, freeze-substitution, TEM, and confocal microscopy. We found that P. kofoidii possessed six nuclear tunnels, which were continuous with a reticulating network of membranes that has thus far gone unnoticed. These membranous extensions interconnect the six tunnels while ramifying throughout the nucleus to form a "nuclear net." To our knowledge, the nuclear net is the most elaborate endomembrane structure described within a nucleus. Our findings demonstrate the utility of tomographic approaches for detecting 3D membrane networks and show that nuclear complexity has been underestimated in Polykrikos kofoidii and, potentially, in other dinoflagellates.
Subject(s)
Chromosome Segregation/physiology , Dinoflagellida/physiology , Nuclear Envelope/physiology , Spindle Apparatus/physiology , Dinoflagellida/metabolism , Endoplasmic Reticulum/physiology , Microscopy, Confocal , Microscopy, Electron, Scanning/methods , Microscopy, Electron, Transmission , Mitosis/physiologyABSTRACT
Symbioses between phototrophs and heterotrophs (a.k.a 'photosymbioses') are extremely common, and range from loose and temporary associations to obligate and highly specialized forms. In the history of life, the most transformative was the 'primary endosymbiosis,' wherein a cyanobacterium was engulfed by a eukaryote and became genetically integrated as a heritable photosynthetic organelle, or plastid. By allowing the rise of algae and plants, this event dramatically altered the biosphere, but its remote origin over one billion years ago has obscured the sequence of events leading to its establishment. Here, we review the genetic, physiological and developmental hurdles involved in early primary endosymbiosis. Since we cannot travel back in time to witness these evolutionary junctures, we will draw on examples of unicellular eukaryotes (protists) spanning diverse modes of photosymbiosis. We also review experimental approaches that could be used to recreate aspects of early primary endosymbiosis on a human timescale.
Subject(s)
Biological Evolution , Cyanobacteria/physiology , Eukaryota/physiology , Plastids/physiology , Symbiosis , Cyanobacteria/genetics , Directed Molecular Evolution , Eukaryota/genetics , Genetic Engineering , Humans , PhotosynthesisABSTRACT
Coevolution is a major driver of speciation in many host-associated symbionts. In the termite-protist digestive symbiosis, the protists are vertically inherited by anal feeding among nest mates. Lower termites (all termite families except Termitidae) and their symbionts have broadly co-diversified over ~170 million yr. However, this inference is based mainly on the restricted distribution of certain protist genera to certain termite families. With the exception of one study, which demonstrated congruent phylogenies for the protist Pseudotrichonympha and its Rhinotermitidae hosts, coevolution in this symbiosis has not been investigated with molecular methods. Here we have characterized the hindgut symbiotic protists (Phylum Parabasalia) across the genus Zootermopsis (Archotermopsidae) using single cell isolation, molecular phylogenetics, and high-throughput amplicon sequencing. We report that the deepest divergence in the Zootermopsis phylogeny (Zootermopsis laticeps [Banks; Isoptera: Termopsidae]) corresponds with a divergence in three of the hindgut protist species. However, the crown Zootermopsis taxa (Zootermopsis angusticollis [Hagen; Isoptera: Termopsidae], Z. nevadensis nevadensis [Hagen; Isoptera: Termopsidae], and Z. nevadensis nuttingi [Haverty & Thorne; Isoptera: Termopsidae]) share the same protist species, with no evidence of co-speciation under our methods. We interpret this pattern as incomplete co-cladogenesis, though the possibility of symbiont exchange cannot be entirely ruled out. This is the first molecular evidence that identical communities of termite-associated protist species can inhabit multiple distinct host species.