40 research outputs found
Phylogenomic Insights into the Origin of Primary Plastids
No full textAbstract 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.
Author Correction: A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids
No full textA molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids
No full textIn 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
eine Analyse von Ultrastruktur, Phylogenie und Kospeziation
No full textThe complex mechanisms leading to a tripartite symbiosis involving bacteria,
flagellates, and host termites are not yet fully understood. While the
flagellates are known to play a major role in the degradation of the
cellulosic food of the termites, in most cases, the functions of the diverse
flagellate-associated bacteria are completely obscure. Unambiguous
identification of the mostly uncultivable prokaryotes and eukaryotes is an
important step in understanding the mutual interactions between the two
partners. For this purpose, in the studies described in my thesis,
morphological investigations (light microscopy and electron microscopy) were
combined with molecular phylogenetic analyses (full-cycle-rRNA approach). In
two earlier light microscopy studies, other authors reported contradicting
numbers of devescovinid flagellates occurring in the hindgut of the dry-wood
termite Incisitermes marginipennis. We clearly and unambiguously documented
the presence of only one devescovinid species (Metadevescovina modica)
inhabiting the gut of I. marginipennis using a combination of various light
and electron microscopy techniques and molecular phylogenetic analysis of the
small subunit (SSU) rRNA gene sequences. Moreover, we confirmed the validity
of the genus Metadevescovina, which had long been discussed as being the same
as the genus Devescovina; monophyly of each of the genera was revealed by
molecular phylogenetic analyses. Metadevescovina could not be distinguished
from Devescovina solely by morphological characteristics of the flagellates
themselves, but the two flagellate genera could be differentiated by examining
their bacterial symbionts. The cell surface of Metadevescovina flagellates is
densely colonized with spirochetes, and that of Devescovina flagellates is
densely covered with filamentous bacteria affiliated to the Bacteroidales.
Molecular phylogenetic analyses of Devescovina spp. and their bacterial
symbionts from a wide range of Kalotermitidae revealed that the termites
acquired two bacterial symbionts by two different routes: vertical
transmission and horizontal transmission. The ectosymbionts of Devescovina
spp. form a monophyletic group within the Bacteroidales (“Candidatus
Armantifilum devescovinae”). Congruence analyses of the phylogenetic trees of
Devescovina spp. and “Candidatus Armantifilum devescovinae” documented a
strict cospeciation of the partners, which indicated an obligate symbiosis,
leading to a vertical transmission of the bacteria within their host lineages.
The ‘Endomicrobia’ endosymbionts of Devescovina spp. are most closely related
to endosymbionts of phylogenetically unrelated termite gut flagellates, which
indicated that these symbionts were acquired by horizontal transmission
between different flagellate species present in the same termite gut. In a
further study documented in this thesis, the multiple symbionts of the
flagellate Joenia annectens from the dry-wood termite Kalotermes flavicollis
were identified, localized using a full-cycle-rRNA approach, and
morphologically described at the ultrastructural level. Two populations of J.
annectens could be distinguished not only by their SSU rRNA gene sequences
(0.8% sequence divergence), but also by differences in their assemblages of
bacterial symbionts. Each of the flagellate populations hosted
phylogenetically distinct ectosymbionts from the phylum Bacteroidetes, while a
single phylotype of ‘Endomicrobia’ was consistently associated with only one
of the host phylotypes. However, not all individuals were colonized, once
again corroborating that ‘Endomicrobia’ are not always cospeciating with their
host lineages. The results reported in my thesis provide important information
about the specificity of the symbioses between termite gut flagellates and
their bacterial symbionts. This information is necessary for further studies
of the function of these symbioses. A possible involvement of bacterial
symbionts in the nitrogen metabolism of the host flagellates is discussed.Die komplexen Mechanismen, welche der Dreiersymbiose zwischen Bakterien,
Flagellaten und ihren Wirtstermiten zugrundeliegen, sind bis heute noch
weitgehend unverstanden. Während den Flagellaten eine wesentliche Rolle beim
Abbau der cellulosehaltigen Nahrung der Termiten zugeschrieben wird, sind die
Funktionen der diversen, mit den Flagellaten assoziierten Bakterien in den
meisten Fällen komplett unbekannt. Ein wichtiger Schritt für die Erforschung
der wechselseitigen Beziehungen zwischen den in der Regel nicht kultivierbaren
pro- und eukaryotischen Symbionten stellt deren eindeutige Identifizierung
dar. Dazu wurden in den vorliegenden Studien morphologische Untersuchungen
(Licht- und Elektronenmikroskopie) beider Partner mit molekular-
phylogenetischen Analysen kombiniert (full-cycle-rRNA approach). In zwei
vorangegangenen lichtmikroskopischen Studien anderer Autoren wurde für die
Trockenholztermite Incisitermes marginipennis eine widersprüchliche
Artenanzahl von devescoviniden Flagellaten dokumentiert. Durch den Einsatz
verschiedener licht- und elektronenmikroskopischer Techniken sowie durch die
Analyse der Sequenzvariabilität der Gene der kleinen ribosomalen Untereinheit
(SSU rRNA) konnten wir in der vorliegenden Arbeit eindeutig zeigen, dass I.
marginipennis lediglich eine Art devescovinider Flagellaten (Metadevescovina
modica) im Darm beherbergt. Gleichzeitig konnten wir die Gültigkeit der
Gattung Metadevescovina, welche bis zum heutigen Tag stark umstritten war und
häufig als Synonym zu Devescovina angesehen wurde, bestätigen.
Molekularphylogenetische Analysen zeigten, dass beide Gattungen jeweils eine
separate monophyletische Gruppe bilden. Eine Unterscheidung der beiden
Gattungen an Hand morphologischer Merkmale der Flagellaten selbst war nicht
möglich, konnte jedoch unter Berücksichtigung ihrer bakteriellen Symbionten
erfolgen. Während Flagellaten der Gattung Metadevescovina einen dichten Besatz
von Spirochaeten auf ihrer Oberfläche zeigen, sind Devescovina spp.
vollständig von filamentösen Bakterien bedeckt, welche den Bacteroidales
zugeordnet werden. Molekularphylogenetische Analysen von Devescovina spp. von
verschiedenen Vertretern der Kalotermitidae und ihren bakteriellen Symbionten
ergaben zwei verschiedene Szenarien bezüglich des Erwerbs dieser Symbionten:
Eine vertikale Weitergabe und eine horizontale Weitergabe. Es konnte gezeigt
werden, dass die Ektosymbionten eine monophyletische Gruppe innerhalb der
Bacteroidales bilden („Candidatus Armantifilum devescovinae“).
Kongruenzanalysen der Stammbäume von Devescovina spp. und „Candidatus
Armantifilum devescovinae“ dokumentierten eine strikte Kospeziation der
Partner. Eine obligate Symbiose der beiden Partner, und somit eine vertikale
Weitergabe der Bakterien innerhalb ihrer Wirtsflagellaten, konnte demnach
belegt werden. Der Erwerb von Symbionten durch horizontale Weitergabe von
anderen Wirtsflagellaten wurde dagegen für die im Zytoplasma vorkommenden
‚Endomicrobia‘ dokumentiert. Hier waren die nächsten Verwandten der mit den
Devescovina spp. assoziierten ‚Endomicrobia‘ Endosymbionten von phylogenetisch
nicht verwandten Termitenflagellaten. In einer weiteren Studie dieser Arbeit
wurden die multiplen Symbionten des Flagellaten Joenia annectens aus der
Trockenholztermite Kalotermes flavicollis identifiziert und lokalisiert (full-
cycle-rRNA approach). Ultrastrukturelle Untersuchungen ermöglichten eine
morphologische Beschreibung der gefundenen Phylotypen. Basierend auf den
Assoziationen mit phylogenetisch verschiedenen Symbionten konnten zwei
Populationen von J. annectens unterschieden werden. Gestützt wurde das
Ergebnis durch die Analyse der SSU rRNA Gensequenzen von J. annectens (0,8%
Sequenzunterschied zwischen beiden Populationen). Beide
Flagellatenpopulationen waren jeweils mit eigenen Ektosymbionten des Phylums
Bacteroidetes assoziiert. Dahingegen beherbergte nur eine der beiden
Populationen von J. annectens einen Vertreter der ‚Endomicrobia‘ im
Zytoplasma. Das Fehlen von ‚Endomicrobia‘-Symbionten bei vielen Flagellaten
der gleichen Population zeigt ein weiteres Beispiel dafür, dass diese
Symbionten nicht immer mit ihren Wirtsflagellaten kospeziieren. Die Ergebnisse
meiner Arbeit haben wichtige Erkenntnisse zur Spezifität der Symbiosen
zwischen Termitenflagellaten und ihrer bakteriellen Symbionten gebracht. Sie
stellen somit eine Grundvoraussetzung für die anstehende Erforschung der
funktionellen Aspekte dieser Symbiosen dar. Eine Beteiligung der bakteriellen
Symbionten am Stickstoffstoffwechsel der Flagellaten wird diskutiert
Early Diversification of Membrane Intrinsic Proteins (MIPs) in Eukaryotes
No full textAbstract Membrane intrinsic proteins (MIPs), including aquaporins (AQPs) and aquaglyceroporins (GLPs), form an ancient family of transporters for water and small solutes across biological membranes. The evolutionary history and functions of MIPs have been extensively studied in vertebrates and land plants, but their widespread presence across the eukaryotic tree of life suggests both a more complex evolutionary history and a broader set of functions than previously thought. That said, the early evolution of MIPs remains obscure. The presence of one GLP and four AQP clades across both bacteria and archaea suggests that the first eukaryotes could have possessed up to five MIPs. Here, we report on a previously unknown richness in MIP diversity across all major eukaryotic lineages, including unicellular eukaryotes, which make up the bulk of eukaryotic diversity. Three MIP clades have likely deep evolutionary origins, dating back to the last eukaryotic common ancestor (LECA), and support the presence of a complex MIP repertoire in early eukaryotes. Overall, our findings highlight the growing complexity of the reconstructed LECA genome: the dynamic evolutionary history of MIPs was set in motion when eukaryotes were in their infancy followed by radiative bursts across all main eukaryotic lineages.Open-Access-Publikationsfonds 202
Predatory colponemids are the sister group to all other alveolates
No full textAlveolates are a major supergroup of eukaryotes encompassing more than ten thousand free-living and parasitic species, including medically, ecologically, and economically important apicomplexans, dinoflagellates, and ciliates. These three groups are among the most widespread eukaryotes on Earth, and their environmental success can be linked to unique innovations that emerged early in each group. Understanding the emergence of these well-studied and diverse groups and their innovations has relied heavily on the discovery and characterization of early-branching relatives, which allow ancestral states to be inferred with much greater confidence. Here we report the phylogenomic analyses of 313 eukaryote protein-coding genes from transcriptomes of three members of one such group, the colponemids (Colponemidia), which support their monophyly and position as the sister lineage to all other known alveolates. Colponemid-related sequences from environmental surveys and our microscopical observations show that colponemids are not common in nature, but they are diverse and widespread in freshwater habitats around the world. Studied colponemids possess two types of extrusive organelles (trichocysts or toxicysts) for active hunting of other unicellular eukaryotes and potentially play an important role in microbial food webs. Colponemids have generally plesiomorphic morphology and illustrate the ancestral state of Alveolata. We further discuss their importance in understanding the evolution of alveolates and the origin of myzocytosis and plastids
Single cell genomics of uncultured marine alveolates shows paraphyly of basal dinoflagellates
No full textMarine alveolates (MALVs) are diverse and widespread early-branching dinoflagellates, but most knowledge of the group comes from a few cultured species that are generally not abundant in natural samples, or from diversity analyses of PCR-based environmental SSU rRNA gene sequences. To more broadly examine MALV genomes, we generated single cell genome sequences from seven individually isolated cells. Genes expected of heterotrophic eukaryotes were found, with interesting exceptions like presence of proteorhodopsin and vacuolar H+-pyrophosphatase. Phylogenetic analysis of concatenated SSU and LSU rRNA gene sequences provided strong support for the paraphyly of MALV lineages. Dinoflagellate viral nucleoproteins were found only in MALV groups that branched as sister to dinokaryotes. Our findings indicate that multiple independent origins of several characteristics early in dinoflagellate evolution, such as a parasitic life style, underlie the environmental diversity of MALVs, and suggest they have more varied trophic modes than previously thought
Phylogenomic Insights into the Origin of Primary Plastids
No full textThe 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.</p
New nephridiophagid genera (Fungi, Chytridiomycota) in a mallow beetle and an earwig
No full textNephridiophagids are unicellular fungi (Chytridiomycota) that infect the Malpighian tubules of insects. Most species have been found in cockroach hosts and belong to the genus Nephridiophaga. Three additional genera have been described from beetles and an earwig. Here, we characterise morphologically and molecular phylogenetically the nephridiophagids of the European earwig Forficula auricularia and the mallow beetle Podagrica malvae. 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 (Nephridiochytrium forficulae gen. nov. et sp. nov.) forms a sister lineage of the Nephridiophaga cluster, the mallow beetle nephridiophagid (Malpighivinco podagricae gen. nov. et sp. nov.) 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
New nephridiophagid genera (Fungi, Chytridiomycota) in a mallow beetle and an earwig
No full textNephridiophagids are unicellular fungi (Chytridiomycota) that infect the Malpighian tubules of insects. Most species have been found in cockroach hosts and belong to the genus Nephridiophaga. Three additional genera have been described from beetles and an earwig. Here, we characterise morphologically and molecular phylogenetically the nephridiophagids of the European earwig Forficula auricularia and the mallow beetle Podagrica malvae. 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 (Nephridiochytrium forficulae gen. nov. et sp. nov.) forms a sister lineage of the Nephridiophaga cluster, the mallow beetle nephridiophagid (Malpighivinco podagricae gen. nov. et sp. nov.) 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
