Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes

Lax, Gordon; Eglit, Yana; Eme, Laura; Bertrand, Erin M.; Roger, Andrew J.; Simpson, Alastair G. B.

doi:10.1038/s41586-018-0708-8

Cited by 106 publications

(152 citation statements)

References 55 publications

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“…Our analyses consistently recovered the monophyly of Archaeplastida with both ML and BI methods, in contrast to recent reports of conflicting ML and BI hypotheses (Brown et al 2018;Gawryluk et al 2019;Strassert et al 2019). The monophyly of Archaeplastida has also been recovered in two recent studies (Lax et al 2018;Price et al 2019) although these are a minority among the datasets with a broad sampling of the eukaryotic diversity (Hampl et al 2009;Baurain et al 2010;Parfrey et al 2010;Burki et al 2012Burki et al , 2016Brown et al 2013;Yabuki et al 2014;Janouškovec et al 2017). In our analyses, Cryptista was the sister group to Archaeplastida, a result that contrasts with previous studies that found it branching within Archaeplastida (Burki et al 2016) or as sister to Haptophyta (Brown et al 2018).…”

Section: Implications For Eukaryotic Evolutionsupporting

confidence: 49%

“…This is because inferring the relationships among PPE necessarily involves resolving the relationships among other deep-branching eukaryotic groups such as Cryptophyta or Haptophyta, all notoriously difficult to place in the eukaryotic tree (Burki et al 2020). With a few exceptions (Lax et al 2018;Price et al 2019), the majority of nuclear phylogenomic studies have not recovered the monophyly of PPE (Hampl et al 2009;Baurain et al 2010;Parfrey et al 2010;Burki et al 2012Burki et al , 2016Brown et al 2013;Yabuki et al 2014;Janouškovec et al 2017), or did so with low statistical support (Burki et al 2007(Burki et al , 2009, or using a very sparse taxon sampling (Rodríguez-Ezpeleta et al 2005, 2007aDeschamps and Moreira 2009). Recent studies reported contradicting Bayesian and maximum likelihood trees regarding Archaeplastida monophyly (Brown et al 2018;Gawryluk et al 2019;Strassert et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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Phylogenomic Insights into the Origin of Primary Plastids

Irisarri

Strassert

Burki

2020

Preprint

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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 a cyanobacterium, presumably in a common ancestor of all 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, the monophyly of both plastid and host (nuclear) genomes is required to support a single ancestral endosymbiosis, whereas non-monophyletic hosts could be explained under scenarios of independent or serial eukaryote-to-eukaryote endosymbioses. Here, we assessed the strength of the signal for the Archaeplastida host monophyly in four available phylogenomic datasets. The effect of phylogenetic methodology, data quality, alignment trimming strategy, gene and taxon sampling, and the presence of outlier genes loci were investigated. Our analyses revealed a general lack of support for host monophyly in the shorter individual datasets. However, when analyzed together under rigorous data curation and complex mixture evolutionary models, the combined dataset consistently recovered the monophyly of Archaeplastida hosts. This study represents an important step towards better understanding the eukaryotic evolution and the origin of plastids.

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Section: Implications For Eukaryotic Evolutionsupporting

confidence: 49%

Section: Introductionmentioning

confidence: 99%

Phylogenomic Insights into the Origin of Primary Plastids

Irisarri

Strassert

Burki

2020

Preprint

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“…Preparing phylogenomic data has been greatly advanced by the recent technological improvements in sequencing that generate a large amount of molecular data at an affordable cost and in a reasonable time-frame (Bleidorn 2016; Vincent et al 2017). Further, some recent phylogenomic analyses have included uncultured microbial eukaryotes (e.g., Lax et al 2018), since the libraries for sequencing of the whole-genome/transcriptome can be prepared from a small number of cells (or even a single cell) isolated from an environment sample (Kolisko et al 2014; Strassert et al 2019).…”

Section: Introductionmentioning

confidence: 99%

“…A large number of extant microbial eukaryotes have never been examined using transcriptomic or genomic techniques, and some of them may hold the keys to resolving important unanswered questions in eukaryotic phylogeny and evolution. Thus, to reconstruct the evolutionary relationships among the major eukaryotic assemblages to a resolution that is both accurate and informative, the taxon sampling in phylogenomic analyses has been improved by targeting two classes of organisms: (i) Novel microbial eukaryotes that represent lineages that were previously unknown to science, and (ii) “orphan eukaryotes” that had been reported before, but whose evolutionary affiliations were unresolved by morphological examinations and/or single-gene phylogenies (Zhao et al 2012; Kamikawa et al 2014; Yabuki et al 2014; Burki et al 2016; Janouškovec et al 2017; Brown et al 2018; Lax et al 2018; Gawryluk et al 2019; Strassert et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Barthelonids represent a deep-branching Metamonad clade with mitochondrion-related organelles generating no ATP

Yazaki

Kume

Shiratori

et al. 2019

Preprint

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23Running head: Phylogeny and putative MRO functions in a new metamonad clade. 25Abstract 28 We here report the phylogenetic position of barthelonids, small anaerobic flagellates 29 previously examined using light microscopy alone. Barthelona spp. were isolated from 30 geographically distinct regions and we established five laboratory strains. Transcriptomic data 31 generated from one Barthelona strain (PAP020) was used for large-scale, multi-gene 32 phylogenetic (phylogenomic) analyses. Our analyses robustly placed strain PAP020 at the 33 base of the Fornicata clade, indicating that barthelonids represent a deep-branching 34 Metamonad clade. Considering the anaerobic/microaerophilic nature of barthelonids and 35 preliminary electron microscopy observations on strain PAP020, we suspected that 36 barthelonids possess functionally and structurally reduced mitochondria (i.e. mitochondrion-37 related organelles or MROs). The metabolic pathways localized in the MRO of strain PAP020 38 were predicted based on its transcriptomic data and compared with those in the MROs of 39 fornicates. Strain PAP020 is most likely incapable of generating ATP in the MRO, as no 40 mitochondrial/MRO enzymes involved in substrate-level phosphorylation were detected. 41 Instead, we detected the putative cytosolic ATP-generating enzyme (acetyl-CoA synthetase), 42 suggesting that strain PAP020 depends on ATP generated in the cytosol. We propose two 43 separate losses of substrate-level phosphorylation from the MRO in the clade containing 44 barthelonids and (other) fornicates.45 46

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“…The members of the group are mostly free-living and predatory to other microbes in soil, sediment, water column and soft water environment, and have highly distinctive morphology. Based on recent studies of transcriptome sequences of two members of the group, an un-rooted gene tree using 351 common genes was constructed, and reported that Hemimastigophoras form a new “supra-kingdom” at the basal position of the Animal kingdom (26). Our genome ToL is showing the group as a member of the protist subgroup of PR-A, which is the basal or sister clade to Majorgroup Animals.…”

Section: Resultsmentioning

confidence: 99%

Genome Tree of Life:Deep Burstof Organism Diversity

Choi

Kim

2019

Preprint

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An organism Tree of Life (organism ToL) is a conceptual and metaphorical tree to capture a simplified narrative of the evolutionary course and kinship among the extant organisms of today. Such tree cannot be experimentally validated but may be reconstructed based on characteristics associated with the extant organisms. Since the whole genome sequence of an organism is, at present, the most comprehensive descriptor of the organism, a genome Tol can be an empirically derivable surrogate for the organism ToL. However, a genome ToL has been impossible to construct because of the practical reasons that experimentally determining the whole genome sequences of a large number of diverse organisms was technically impossible. Thus, for several decades, gene ToLs, based on selected genes, have been commonly used as a surrogate for the organisms ToL. This situation changed dramatically during the last several decades due to rapid advances in DNA sequencing technology. Here we describe the main features of a genome ToL that are different from those of the broadly accepted gene ToLs: (a) the first two organism groups to emerge are the founders of prokarya and eukarya, (b) they diversify into six large groups and all the founders of the groups have emerged in a “Deep Burst” at the very beginning period of the emergence of Life on Earth and (c) other differences are notable in the order of emergence of smaller groups.Significance StatementTree of Life is a conceptual and metaphorical tree that captures a simplified narrative of the evolutionary course and kinship among all living organisms of today. Since the whole genome sequence information of an organism is, at present, the most comprehensive description of the organism, we reconstructed a Genome Tree of Life using the proteome information from the whole genomes of over 4000 different living organisms on Earth. It suggests that (a) the first two primitive organism groups to emerge are the founders of prokarya and eukarya, (b) they diversify into six large groups, and (c) all the founders of the groups have emerged in a “Deep Burst” at the very beginning period of the emergence of Life on Earth.

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Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes

Cited by 106 publications

References 55 publications

Phylogenomic Insights into the Origin of Primary Plastids

Phylogenomic Insights into the Origin of Primary Plastids

Barthelonids represent a deep-branching Metamonad clade with mitochondrion-related organelles generating no ATP

Genome Tree of Life:Deep Burstof Organism Diversity

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