In modern oceans, eukaryotic phytoplankton is dominated by lineages with red algal-derived plastids such as diatoms, dinoflagellates, and coccolithophores. Despite the ecological importance of these ...groups and many others representing a huge diversity of forms and lifestyles, we still lack a comprehensive understanding of their evolution and how they obtained their plastids. New hypotheses have emerged to explain the acquisition of red algal-derived plastids by serial endosymbiosis, but the chronology of these putative independent plastid acquisitions remains untested. Here, we establish a timeframe for the origin of red algal-derived plastids under scenarios of serial endosymbiosis, using Bayesian molecular clock analyses applied on a phylogenomic dataset with broad sampling of eukaryote diversity. We find that the hypotheses of serial endosymbiosis are chronologically possible, as the stem lineages of all red plastid-containing groups overlap in time. This period in the Meso- and Neoproterozoic Eras set the stage for the later expansion to dominance of red algal-derived primary production in the contemporary oceans, which profoundly altered the global geochemical and ecological conditions of the Earth.
Phylogenomic analyses of hundreds of protein-coding genes aimed at resolving phylogenetic relationships is now a common practice. However, no software currently exists that includes tools for dataset ...construction and subsequent analysis with diverse validation strategies to assess robustness. Furthermore, there are no publicly available high-quality curated databases designed to assess deep (>100 million years) relationships in the tree of eukaryotes. To address these issues, we developed an easy-to-use software package, PhyloFisher (
https://github.com/TheBrownLab/PhyloFisher
), written in Python 3. PhyloFisher includes a manually curated database of 240 protein-coding genes from 304 eukaryotic taxa covering known eukaryotic diversity, a novel tool for ortholog selection, and utilities that will perform diverse analyses required by state-of-the-art phylogenomic investigations. Through phylogenetic reconstructions of the tree of eukaryotes and of the Saccharomycetaceae clade of budding yeasts, we demonstrate the utility of the PhyloFisher workflow and the provided starting database to address phylogenetic questions across a large range of evolutionary time points for diverse groups of organisms. We also demonstrate that undetected paralogy can remain in phylogenomic “single-copy orthogroup” datasets constructed using widely accepted methods such as all vs. all BLAST searches followed by Markov Cluster Algorithm (MCL) clustering and application of automated tree pruning algorithms. Finally, we show how the PhyloFisher workflow helps detect inadvertent paralog inclusions, allowing the user to make more informed decisions regarding orthology assignments, leading to a more accurate final dataset.
Nephridiophagids are unicellular eukaryotes that parasitize the Malpighian tubules of numerous insects. Their life cycle comprises multinucleate vegetative plasmodia that divide into oligonucleate ...and uninucleate cells, and sporogonial plasmodia that form uninucleate spores. Nephridiophagids are poor in morphological characteristics, and although they have been tentatively identified as early-branching fungi based on the SSU rRNA gene sequences of three species, their exact position within the fungal tree of live remained unclear. In this study, we describe two new species of nephridiophagids (Nephridiophaga postici and Nephridiophaga javanicae) from cockroaches. Using long-read sequencing of the nearly complete rDNA operon of numerous further species obtained from cockroaches and earwigs to improve the resolution of the phylogenetic analysis, we found a robust affiliation of nephridiophagids with the Chytridiomycota-a group of zoosporic fungi that comprises parasites of diverse host taxa, such as microphytes, plants, and amphibians. The presence of the same nephridiophagid species in two only distantly related cockroaches indicates that their host specificity is not as strict as generally assumed.
The endosymbiotic origin of plastids from cyanobacteria gave eukaryotes photosynthetic capabilities and launched the diversification of countless forms of algae. These primary plastids are found in ...members of the eukaryotic supergroup Archaeplastida. All known archaeplastids still retain some form of primary plastids, which are widely assumed to have a single origin. Here, we use single-cell genomics from natural samples combined with phylogenomics to infer the evolutionary origin of the phylum Picozoa, a globally distributed but seemingly rare group of marine microbial heterotrophic eukaryotes. Strikingly, the analysis of 43 single-cell genomes shows that Picozoa belong to Archaeplastida, specifically related to red algae and the phagotrophic rhodelphids. These picozoan genomes support the hypothesis that Picozoa lack a plastid, and further reveal no evidence of an early cryptic endosymbiosis with cyanobacteria. These findings change our understanding of plastid evolution as they either represent the first complete plastid loss in a free-living taxon, or indicate that red algae and rhodelphids obtained their plastids independently of other archaeplastids.
The resolution of the broad-scale tree of eukaryotes is constantly improving, but the evolutionary origin of several major groups remains unknown. Resolving the phylogenetic position of these ..."orphan" groups is important, especially those that originated early in evolution, because they represent missing evolutionary links between established groups. Telonemia is one such orphan taxon for which little is known. The group is composed of molecularly diverse biflagellated protists, often prevalent although not abundant in aquatic environments. Telonemia has been hypothesized to represent a deeply diverging eukaryotic phylum but no consensus exists as to where it is placed in the tree. Here, we established cultures and report the phylogenomic analyses of three new transcriptome data sets for divergent telonemid lineages. All our phylogenetic reconstructions, based on 248 genes and using site-heterogeneous mixture models, robustly resolve the evolutionary origin of Telonemia as sister to the Sar supergroup. This grouping remains well supported when as few as 60% of the genes are randomly subsampled, thus is not sensitive to the sets of genes used but requires a minimal alignment length to recover enough phylogenetic signal. Telonemia occupies a crucial position in the tree to examine the origin of Sar, one of the most lineage-rich eukaryote supergroups. We propose the moniker "TSAR" to accommodate this new mega-assemblage in the phylogeny of eukaryotes.
Abstract
The origin of plastids was a major evolutionary event that paved the way for an astonishing diversification of photosynthetic eukaryotes. Plastids originated by endosymbiosis between a ...heterotrophic eukaryotic host and cyanobacteria, presumably in a common ancestor of the primary photosynthetic eukaryotes (Archaeplastida). A single origin of primary plastids is well supported by plastid evidence but not by nuclear phylogenomic analyses, which have consistently failed to recover the monophyly of Archaeplastida hosts. Importantly, plastid monophyly and nonmonophyletic hosts could be explained under scenarios of independent or serial eukaryote-to-eukaryote endosymbioses. Here, we assessed the strength of the signal for the monophyly of Archaeplastida hosts in four available phylogenomic data sets. The effect of phylogenetic methodology, data quality, alignment trimming strategy, gene and taxon sampling, and the presence of outlier genes were investigated. Our analyses revealed a lack of support for host monophyly in the shorter individual data sets. However, when analyzed together under rigorous data curation and complex mixture models, the combined nuclear data sets supported the monophyly of primary photosynthetic eukaryotes (Archaeplastida) and recovered a putative association with plastid-lacking Picozoa. This study represents an important step toward better understanding deep eukaryotic evolution and the origin of plastids. Archaeplastida; Bayesian; chloroplast; maximum likelihood; mixture model; ortholog; outlier loci; paralog; protist.
Summary
Termite gut flagellates are typically colonized by specific bacterial symbionts. Here we describe the phylogeny, ultrastructure and subcellular location of ‘Candidatus Adiutrix ...intracellularis’, an intracellular symbiont of Trichonympha collaris in the termite Zootermopsis nevadensis. It represents a novel, deep‐branching clade of uncultured Deltaproteobacteria widely distributed in intestinal tracts of termites and cockroaches. Fluorescence in situ hybridization and transmission electron microscopy localized the endosymbiont near hydrogenosomes in the posterior part and near the ectosymbiont ‘Candidatus Desulfovibrio trichonymphae’ in the anterior part of the host cell. The draft genome of ‘Ca. Adiutrix intracellularis’ obtained from a metagenomic library revealed the presence of a complete gene set encoding the Wood–Ljungdahl pathway, including two homologs of fdhF encoding hydrogenase‐linked formate dehydrogenases (FDHH) and all other components of the recently described hydrogen‐dependent carbon dioxide reductase (HDCR) complex, which substantiates previous claims that the symbiont is capable of reductive acetogenesis from CO2 and H2. The close phylogenetic relationship between the HDCR components and their homologs in homoacetogenic Firmicutes and Spirochaetes suggests that the deltaproteobacterium acquired the capacity for homoacetogenesis via lateral gene transfer. The presence of genes for nitrogen fixation and the biosynthesis of amino acids and cofactors indicate the nutritional nature of the symbiosis.
Termites digest lignocellulose with the help of their symbiotic gut microbiota. In the hindgut of evolutionary lower termites, a dense community of cellulolytic flagellates sequesters wood particles ...from the hindgut content into their digestive vacuoles. In higher termites (family Termitidae), which possess an entirely prokaryotic microbiota, the wood particles are available for bacterial colonization. Substantial particle‐associated cellulase activities have been detected in the hindgut of Nasutitermes species, but the microorganisms responsible for these activities and their potential association with the wood fibres remain to be studied. Here, we used density‐gradient centrifugation to separate wood fibres and adherent bacterial cells from cells freely suspended in the hindgut fluid. In Nasutitermes corniger, the fibre fraction contained 28% of the DNA and 45% of the cellulase activity in the luminal contents (P3 region). Community fingerprinting (terminal restriction fragment length polymorphism) and pyrotag sequencing analysis of the bacterial 16S rRNA genes demonstrated that the wood fibres in the hindgut of both N. corniger and N. takasagoensis are specifically colonized by members of Fibrobacteres, the TG3 phylum, and certain lineages of Spirochaetes characteristic of the gut microbiota of wood‐feeding higher termites. We propose that the loss of flagellates in higher termites provided a new niche for fibre‐associated cellulolytic bacteria.
Phylogenomic analyses have boosted our understanding of the evolutionary trajectories of all living forms by providing continuous improvements to the tree of life.1,2,3,4,5 Within this tree, fungi ...represent an ancient eukaryote group,6 having diverged from the animals ∼1.35 billion years ago.7 Estimates of the number of extant species range between 1.5 and 3.8 million.8,9 Recent reclassifications and the discovery of the deep-branching Sanchytriomycota lineage10 have brought the number of proposed phyla to 20,11 21 if the Microsporidia are included.12,13,14 Uncovering how the diverse and globally distributed fungi are related to each other is fundamental for understanding how their lifestyles, morphologies, and metabolic capacities evolved. To date, many of the proposed relationships among the phyla remain controversial and no phylogenomic study has examined the entire fungal tree using a taxonomically comprehensive dataset and suitable models of evolution. We assembled and curated a 299-protein dataset with a taxon sampling broad enough to encompass all recognized fungal diversity with available data, but selective enough to run computationally intensive analyses using best-fitting models. Using a range of reconstruction methods, we were able to resolve many contested nodes, such as a sister relationship of Chytridiomyceta to all other non-Opisthosporidia fungi (with Chytridiomycota being sister to Monoblepharomycota + Neocallimastigomycota), a branching of Blastocladiomycota + Sanchytriomycota after the Chytridiomyceta but before other non-Opisthosporidia fungi, and a branching of Glomeromycota as sister to the Dikarya. Our up-to-date fungal tree of life will serve as a springboard for future investigations on the early evolution of fungi.
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•Phylogenomic study of fungi using a well-curated and taxon-balanced dataset•Branching order among fungal phyla remained consistent across multiple analyses•Only the position of Glomeromycota showed inconsistency•Method validation suggests a sister relationship of Glomeromycota to the Dikarya
Strassert and Monaghan further resolve the early diversification of fungi by analyzing a 299-protein dataset with a taxon sampling broad enough to encompass all recognized fungal diversity with available data, but selective enough to apply computationally intensive tree inference algorithms.
Nephridiophagids are unicellular fungi (Chytridiomycota) that infect the Malpighian tubules of insects. Most species have been found in cockroach hosts and belong to the genus
. Three additional ...genera have been described from beetles and an earwig. Here, we characterise morphologically and molecular phylogenetically the nephridiophagids of the European earwig
and the mallow beetle
. Their morphology and life cycle stages resemble those of other nephridiophagids, but their rRNA gene sequences support the existence of two additional genera. Whereas the earwig nephridiophagid (
) forms a sister lineage of the
cluster, the mallow beetle nephridiophagid (
) represents the earliest divergent lineage within the nephridiophagids, being sister to all other species. Our results corroborate the hypothesis that different insect groups harbour distinct nephridiophagid lineages.
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