scispace - formally typeset
Search or ask a question
Journal ArticleDOI

Between a Pod and a Hard Test: The Deep Evolution of Amoebae.

TL;DR: The results support the hypothesis that the last common ancestor of Amoebozoa was sexual and flagellated, and it also may have had the ability to disperse propagules from a sporocarp-type fruiting body.
Abstract: Amoebozoa is the eukaryotic supergroup sister to Obazoa, the lineage that contains the animals and Fungi, as well as their protistan relatives, and the breviate and apusomonad flagellates. Amoebozoa is extraordinarily diverse, encompassing important model organisms and significant pathogens. Although amoebozoans are integral to global nutrient cycles and present in nearly all environments, they remain vastly understudied. We present a robust phylogeny of Amoebozoa based on broad representative set of taxa in a phylogenomic framework (325 genes). By sampling 61 taxa using culture-based and single-cell transcriptomics, our analyses show two major clades of Amoebozoa, Discosea, and Tevosa. This phylogeny refutes previous studies in major respects. Our results support the hypothesis that the last common ancestor of Amoebozoa was sexual and flagellated, it also may have had the ability to disperse propagules from a sporocarp-type fruiting body. Overall, the main macroevolutionary patterns in Amoebozoa appear to result from the parallel losses of homologous characters of a multiphase life cycle that included flagella, sex, and sporocarps rather than independent acquisition of convergent features.
Citations
More filters
Journal ArticleDOI
TL;DR: It is confirmed that eukaryotes form at least two domains, the loss of monophyly in the Excavata, robust support for the Haptista and Cryptista, and suggested primer sets for DNA sequences from environmental samples that are effective for each clade are provided.
Abstract: This revision of the classification of eukaryotes follows that of Adl et al., 2012 [J. Euk. Microbiol. 59(5)] and retains an emphasis on protists. Changes since have improved the resolution of many ...

750 citations

Journal ArticleDOI
TL;DR: The combination of traditional culturing with maturing culture-free approaches and phylogenomics should accelerate the process of completing and resolving the eukaryote Tree of Life at its deepest levels.
Abstract: For 15 years, the eukaryote Tree of Life (eToL) has been divided into five to eight major groupings, known as ‘supergroups’. However, the tree has been profoundly rearranged during this time. The new eToL results from the widespread application of phylogenomics and numerous discoveries of major lineages of eukaryotes, mostly free-living heterotrophic protists. The evidence that supports the tree has transitioned from a synthesis of molecular phylogenetics and biological characters to purely molecular phylogenetics. Most current supergroups lack defining morphological or cell-biological characteristics, making the supergroup label even more arbitrary than before. Going forward, the combination of traditional culturing with maturing culture-free approaches and phylogenomics should accelerate the process of completing and resolving the eToL at its deepest levels.

433 citations


Cites background from "Between a Pod and a Hard Test: The ..."

  • ...Large numbers of cells can be isolated en masse from the environment then screened using molecular techniques to identify important organisms for further study [78–83]; alternatively, target cells can be identified by microscopy and selected individually [40,41,61,75]....

    [...]

Journal ArticleDOI
TL;DR: This article provides an outline of the classification of the kingdom Fungi (including fossil fungi), and treats 19 phyla of fungi, including all currently described orders of fungi.
Abstract: This article provides an outline of the classification of the kingdom Fungi (including fossil fungi. i.e. dispersed spores, mycelia, sporophores, mycorrhizas). We treat 19 phyla of fungi. These are Aphelidiomycota, Ascomycota, Basidiobolomycota, Basidiomycota, Blastocladiomycota, Calcarisporiellomycota, Caulochytriomycota, Chytridiomycota, Entomophthoromycota, Entorrhizomycota, Glomeromycota, Kickxellomycota, Monoblepharomycota, Mortierellomycota, Mucoromycota, Neocallimastigomycota, Olpidiomycota, Rozellomycota and Zoopagomycota. The placement of all fungal genera is provided at the class-, order- and family-level. The described number of species per genus is also given. Notes are provided of taxa for which recent changes or disagreements have been presented. Fungus-like taxa that were traditionally treated as fungi are also incorporated in this outline (i.e. Eumycetozoa, Dictyosteliomycetes, Ceratiomyxomycetes and Myxomycetes). Four new taxa are introduced: Amblyosporida ord. nov. Neopereziida ord. nov. and Ovavesiculida ord. nov. in Rozellomycota, and Protosporangiaceae fam. nov. in Dictyosteliomycetes. Two different classifications (in outline section and in discussion) are provided for Glomeromycota and Leotiomycetes based on recent studies. The phylogenetic reconstruction of a four-gene dataset (18S and 28S rRNA, RPB1, RPB2) of 433 taxa is presented, including all currently described orders of fungi.

381 citations


Cites background or methods from "Between a Pod and a Hard Test: The ..."

  • ...To preserve this widely used name, Kang et al. (2017) proposed including in the Eumycetozoa only one group of protostelids, the Protosporangiida, which forms a monophyletic unit with myxomycetes and dictyostelids....

    [...]

  • ...To preserve this widely used name, Kang et al. (2017) proposed including in the Eumycetozoa only one group of protostelids, the Protosporangiida, which forms a monophyletic unit with myxomycetes and dictyostelids. In terms of botanical nomenclature, the Protosporangiida may be considered as the class Ceratiomyxomycota (Leontyev et al. 2019). Therefore, in the classification given below, we recognize three classes within the Eumycetozoa. These are the Dictyosteliomycetes, Ceratiomyxomycetes and Myxomycetes, as outlined by Leontyev et al. (2019)....

    [...]

  • ...This group was initially described under the zoological name Protosporangiida (Kang et al. 2017). The botanical name Ceratiomyxomycetes was proposed by Hawksworth et al. (1983) as nom....

    [...]

  • ...This group was initially described under the zoological name Protosporangiida (Kang et al. 2017). The botanical name Ceratiomyxomycetes was proposed by Hawksworth et al. (1983) as nom. inval. (ICN, Art. 39.1), and later validated by Leontyev et al. (2019)....

    [...]

  • ...All available phylogenies support the placement of these organisms in the supergroup Amoebozoa (Shadwick et al. 2009, Tice et al. 2016, Kang et al. 2017) (Table 2)....

    [...]

Journal ArticleDOI
TL;DR: An overview of the enormous morphological, taxonomical and functional diversity of soil protists is provided, and current challenges and opportunities in soil protistology are discussed.
Abstract: Protists include all eukaryotes except plants, fungi and animals. They are an essential, yet often forgotten, component of the soil microbiome. Method developments have now furthered our understanding of the real taxonomic and functional diversity of soil protists. They occupy key roles in microbial foodwebs as consumers of bacteria, fungi and other small eukaryotes. As parasites of plants, animals and even of larger protists, they regulate populations and shape communities. Pathogenic forms play a major role in public health issues as human parasites, or act as agricultural pests. Predatory soil protists release nutrients enhancing plant growth. Soil protists are of key importance for our understanding of eukaryotic evolution and microbial biogeography. Soil protists are also useful in applied research as bioindicators of soil quality, as models in ecotoxicology and as potential biofertilizers and biocontrol agents. In this review, we provide an overview of the enormous morphological, taxonomical and functional diversity of soil protists, and discuss current challenges and opportunities in soil protistology. Research in soil biology would clearly benefit from incorporating more protistology alongside the study of bacteria, fungi and animals.

297 citations


Cites background from "Between a Pod and a Hard Test: The ..."

  • ...Sporocarps, where a single cell develops into a stalked spore-bearing structure, are unique to Amoebozoa (Kang et al. 2017; Spiegel et al. 2017)....

    [...]

  • ...All sporocarpic and some sorocarpic species are found within the Amoebozoa (Fiore-Donno et al. 2010; Kang et al. 2017; Spiegel et al. 2017), whereas the remainder of the sorocarpic forms are found throughout the whole eukaryotic tree (Brown and Silberman 2013)....

    [...]

  • ...Protosteloid amoebae occur separately in several clades of Amoebozoa suggesting that spore formation might be a synapomorphic character for the entire supergroup Amoebozoa (Kang et al. 2017; Spiegel et al. 2017)....

    [...]

  • ...…Legionella spp. legionnaires’ disease, opportunistic infections Rowbotham 1980 Vibrio cholerae cholera Thom et al. 1992 Dictyostelia and Copromyxa (Kang et al. 2017), but also in several taxa in diverse supergroups such as in one ciliate (Olive and Blanton 1980), Heterolobosea (Brown, Silberman…...

    [...]

  • ...Naegleria Legionella spp. legionnaires’ disease, opportunistic infections Rowbotham 1980 Vibrio cholerae cholera Thom et al. 1992 Dictyostelia and Copromyxa (Kang et al. 2017), but also in several taxa in diverse supergroups such as in one ciliate (Olive and Blanton 1980), Heterolobosea (Brown, Silberman and Spiegel 2010), Opisthokonts (Brown, Spiegel and Silberman 2009), Rhizaria (Brown et al. 2012), and Stramenopiles (Tice et al. 2016)....

    [...]

Journal ArticleDOI
TL;DR: CRuMs and ancyromonads represent two distinct major groups that branch deeply on the lineage that includes animals, near the most commonly inferred root of the eukaryote tree, which makes both groups crucial in examinations of the deepest-level history of extant eucaryotes.
Abstract: Recent phylogenetic analyses position certain "orphan" protist lineages deep in the tree of eukaryotic life, but their exact placements are poorly resolved. We conducted phylogenomic analyses that incorporate deeply sequenced transcriptomes from representatives of collodictyonids (diphylleids), rigifilids, Mantamonas, and ancyromonads (planomonads). Analyses of 351 genes, using site-heterogeneous mixture models, strongly support a novel super-group-level clade that includes collodictyonids, rigifilids, and Mantamonas, which we name "CRuMs". Further, they robustly place CRuMs as the closest branch to Amorphea (including animals and fungi). Ancyromonads are strongly inferred to be more distantly related to Amorphea than are CRuMs. They emerge either as sister to malawimonads, or as a separate deeper branch. CRuMs and ancyromonads represent two distinct major groups that branch deeply on the lineage that includes animals, near the most commonly inferred root of the eukaryote tree. This makes both groups crucial in examinations of the deepest-level history of extant eukaryotes.

92 citations


Cites background from "Between a Pod and a Hard Test: The ..."

  • ...There is considerable debate over the position of the root, however (Cavalier-Smith 2010; Katz et al. 2012; He et al. 2014)....

    [...]

References
More filters
Journal ArticleDOI
TL;DR: It is shown that a combination of hill-climbing approaches and a stochastic perturbation method can be time-efficiently implemented and found higher likelihoods between 62.2% and 87.1% of the studied alignments, thus efficiently exploring the tree-space.
Abstract: Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus, there is need for additional approaches that employ different search strategies to find ML trees and that are at the same time as fast as currently available ML programs. We show that a combination of hill-climbing approaches and a stochastic perturbation method can be time-efficiently implemented. If we allow the same CPU time as RAxML and PhyML, then our software IQ-TREE found higher likelihoods between 62.2% and 87.1% of the studied alignments, thus efficiently exploring the tree-space. If we use the IQ-TREE stopping rule, RAxML and PhyML are faster in 75.7% and 47.1% of the DNA alignments and 42.2% and 100% of the protein alignments, respectively. However, the range of obtaining higher likelihoods with IQ-TREE improves to 73.3-97.1%. IQ-TREE is freely available at http://www.cibiv.at/software/iqtree.

13,668 citations


"Between a Pod and a Hard Test: The ..." refers methods in this paper

  • ...…LGþC4þ FþC60þ PMSF model that similarly estimates site-specific amino acid (AA) Deep Evolution of Amoebae . doi:10.1093/molbev/msx162 MBE profiles for phylogenomic analyses based on the C60 empirical frequency profiles (Le and Gascuel 2008) was used for ML analyses in IQ-Tree (Nguyen et al. 2014)....

    [...]

  • ...To examine this conflict, we estimated the rate of evolution at sites in the supermatrix and progressively removed them in a stepwise fashion, plotting bootstrap values for nodes of interest in the tree per site deletion step under the models LGþC4þ F and LGþC4þ FþC60þ PMSF models estimated in IQ-Tree (fig....

    [...]

  • ...Although the CAT-GTR model cannot be used in the ML framework, the LGþC4þ FþC60þ PMSF model that similarly estimates site-specific amino acid (AA) Deep Evolution of Amoebae . doi:10.1093/molbev/msx162 MBE profiles for phylogenomic analyses based on the C60 empirical frequency profiles (Le and Gascuel 2008) was used for ML analyses in IQ-Tree (Nguyen et al. 2014)....

    [...]

  • ...ML trees were inferred in IQTREE v. 1.5.0 (Nguyen et al. 2014)....

    [...]

Journal ArticleDOI
TL;DR: This method further refine this method by incorporating the variability of evolutionary rates across sites in the matrix estimation and using a much larger and diverse database than BRKALN, which was used to estimate WAG.
Abstract: Amino acid replacement matrices are an essential basis of protein phylogenetics. They are used to compute substitution probabilities along phylogeny branches and thus the likelihood of the data. They are also essential in protein alignment. A number of replacement matrices and methods to estimate these matrices from protein alignments have been proposed since the seminal work of Dayhoff et al. (1972). An important advance was achieved by Whelan and Goldman (2001) and their WAG matrix, thanks to an efficient maximum likelihood estimation approach that accounts for the phylogenies of sequences within each training alignment. We further refine this method by incorporating the variability of evolutionary rates across sites in the matrix estimation and using a much larger and diverse database than BRKALN, which was used to estimate WAG. To estimate our new matrix (called LG after the authors), we use an adaptation of the XRATE software and 3,912 alignments from Pfam, comprising approximately 50,000 sequences and approximately 6.5 million residues overall. To evaluate the LG performance, we use an independent sample consisting of 59 alignments from TreeBase and randomly divide Pfam alignments into 3,412 training and 500 test alignments. The comparison with WAG and JTT shows a clear likelihood improvement. With TreeBase, we find that 1) the average Akaike information criterion gain per site is 0.25 and 0.42, when compared with WAG and JTT, respectively; 2) LG is significantly better than WAG for 38 alignments (among 59), and significantly worse with 2 alignments only; and 3) tree topologies inferred with LG, WAG, and JTT frequently differ, indicating that using LG impacts not only the likelihood value but also the output tree. Results with the test alignments from Pfam are analogous. LG and a PHYML implementation can be downloaded from http://atgc.lirmm.fr/LG

2,615 citations


"Between a Pod and a Hard Test: The ..." refers methods in this paper

  • ...profiles for phylogenomic analyses based on the C60 empirical frequency profiles (Le and Gascuel 2008) was used...

    [...]

  • ...…LGþC4þ FþC60þ PMSF model that similarly estimates site-specific amino acid (AA) Deep Evolution of Amoebae . doi:10.1093/molbev/msx162 MBE profiles for phylogenomic analyses based on the C60 empirical frequency profiles (Le and Gascuel 2008) was used for ML analyses in IQ-Tree (Nguyen et al. 2014)....

    [...]

Journal ArticleDOI
TL;DR: It is shown that the AU test is less biased than other methods in typical cases of tree selection, as well as in the analysis of mammalian mitochondrial protein sequences.
Abstract: An approximately unbiased (AU) test that uses a newly devised multiscale bootstrap technique was developed for general hypothesis testing of regions in an attempt to reduce test bias. It was applied to maximum-likelihood tree selection for obtaining the confidence set of trees. The AU test is based on the theory of Efron et al. (Proc. Natl. Acad. Sci. USA 93:13429-13434; 1996), but the new method provides higher-order accuracy yet simpler implementation. The AU test, like the Shimodaira-Hasegawa (SH) test, adjusts the selection bias overlooked in the standard use of the bootstrap probability and Kishino-Hasegawa tests. The selection bias comes from comparing many trees at the same time and often leads to overconfidence in the wrong trees. The SH test, though safe to use, may exhibit another type of bias such that it appears conservative. Here I show that the AU test is less biased than other methods in typical cases of tree selection. These points are illustrated in a simulation study as well as in the analysis of mammalian mitochondrial protein sequences. The theoretical argument provides a simple formula that covers the bootstrap probability test, the Kishino-Hasegawa test, the AU test, and the Zharkikh-Li test. A practical suggestion is provided as to which test should be used under particular circumstances.

2,452 citations


"Between a Pod and a Hard Test: The ..." refers methods in this paper

  • ...Additionally, constraining the tree with Lobosa (Discoseaþ Tubulinea, with or without Cutosea) can be rejected under approximately unbiased (AU) tests (Shimodaira, 2002) at a confidence interval of 95% using our data set (P-value¼ 0.0059 and 0.0014, respectively, table 1)....

    [...]

  • ...Additionally, constraining the tree with Lobosa (Discoseaþ Tubulinea, with or without Cutosea) can be rejected under approximately unbiased (AU) tests (Shimodaira, 2002) at a confidence interval of 95% using our data set (P-value1⁄4 0....

    [...]

Journal ArticleDOI
TL;DR: This revision of the classification of eukaryotes retains an emphasis on the protists and incorporates changes since 2005 that have resolved nodes and branches in phylogenetic trees.
Abstract: This revision of the classification of eukaryotes, which updates that of Adl et al. [J. Eukaryot. Microbiol. 52 (2005) 399], retains an emphasis on the protists and incorporates changes since 2005 that have resolved nodes and branches in phylogenetic trees. Whereas the previous revision was successful in re-introducing name stability to the classification, this revision provides a classification for lineages that were then still unresolved. The supergroups have withstood phylogenetic hypothesis testing with some modifications, but despite some progress, problematic nodes at the base of the eukaryotic tree still remain to be statistically resolved. Looking forward, subsequent transformations to our understanding of the diversity of life will be from the discovery of novel lineages in previously under-sampled areas and from environmental genomic information.

1,414 citations


"Between a Pod and a Hard Test: The ..." refers background in this paper

  • ...First, Eumycetozoa is the older name such that it even has priority over the entirety of Amoebozoa (see Shadwick et al. 2009; Adl et al. 2012)....

    [...]

  • ...Relatively few amoebozoan lineages have a flagellate state, and all confirmed flagellate taxa are found in Evosea (fig. 3, see supplementary table S1, Supplementary Material online; Spiegel 1991; Spiegel et al. 1995; Mikrjukov and Mylnikov 1998; Smirnov et al. 2011; Adl et al. 2012; Ptackova et al. 2013; Berney et al. 2015; Zadrobilkova et al. 2015; P anek et al. 2016)....

    [...]

  • ...…each contain some species that are flagellated (usually amoeboflagellates sensu Spiegel 1990), and at least some members of all three groups (Adl et al. 2012) have flagella that contain an electron-dense element in their transition zone, a character not found in any other eukaryotes (see…...

    [...]

  • ...Several amoebozoans have life cycles with amoeboid cells that can assume both morphologies at alternate stages (see supplementary table S1, Supplementary Material online), for example, the myxogastrids and some protosteloid amoebae (Olive 1975; Adl et al. 2012)....

    [...]

  • ...For instance, it is possible to conclude that LCAA had a flagellate state in its life history (Spiegel 1991, 2011; Spiegel et al. 1995; Lahr et al. 2011b; Adl et al. 2012; Yubuki and Leander 2013) as this character must have been present in the Last Eukaryote Common Ancestor (LECA; Goodenough and Heitman 2014)....

    [...]

Journal ArticleDOI
Ludwig Eichinger1, Justin A. Pachebat1, Justin A. Pachebat2, Gernot Glöckner, Marie-Adèle Rajandream3, Richard Sucgang4, Matthew Berriman3, J. Song4, Rolf Olsen5, Karol Szafranski, Qikai Xu4, Budi Tunggal1, Sarah K. Kummerfeld2, Martin Madera2, Bernard Anri Konfortov2, Francisco Rivero1, Alan T. Bankier2, Rüdiger Lehmann, N. Hamlin3, Robert L. Davies3, Pascale Gaudet6, Petra Fey6, Karen E Pilcher6, Guokai Chen4, David L. Saunders3, Erica Sodergren4, P. Davis3, Arnaud Kerhornou3, X. Nie4, Neil Hall3, Christophe Anjard5, Lisa Hemphill4, Nathalie Bason3, Patrick Farbrother1, Brian A. Desany4, Eric M. Just6, Takahiro Morio7, René Rost8, Carol Churcher3, J. Cooper3, Stephen F. Haydock9, N. van Driessche4, Ann Cronin3, Ian Goodhead3, Donna M. Muzny4, T. Mourier3, Arnab Pain3, Mingyang Lu4, D. Harper3, R. Lindsay4, Heidi Hauser3, Kylie R. James3, M. Quiles4, M. Madan Babu2, Tsuneyuki Saito10, Carmen Buchrieser11, A. Wardroper12, A. Wardroper2, Marius Felder, M. Thangavelu, D. Johnson3, Andrew J Knights3, H. Loulseged4, Karen Mungall3, Karen Oliver3, Claire Price3, Michael A. Quail3, Hideko Urushihara7, Judith Hernandez4, Ester Rabbinowitsch3, David Steffen4, Mandy Sanders3, Jun Ma4, Yuji Kohara13, Sarah Sharp3, Mark Simmonds3, S. Spiegler3, Adrian Tivey3, Sumio Sugano14, Brian White3, Danielle Walker3, John Woodward3, Thomas Winckler, Yoshiaki Tanaka7, Gad Shaulsky4, Michael Schleicher8, George M. Weinstock4, André Rosenthal, Edward C. Cox15, Rex L. Chisholm6, Richard A. Gibbs4, William F. Loomis5, Matthias Platzer, Robert R. Kay2, Jeffrey G. Williams16, Paul H. Dear2, Angelika A. Noegel1, Bart Barrell3, Adam Kuspa4 
05 May 2005-Nature
TL;DR: A proteome-based phylogeny shows that the amoebozoa diverged from the animal–fungal lineage after the plant–animal split, but Dictyostelium seems to have retained more of the diversity of the ancestral genome than have plants, animals or fungi.
Abstract: The social amoebae are exceptional in their ability to alternate between unicellular and multicellular forms. Here we describe the genome of the best-studied member of this group, Dictyostelium discoideum. The gene-dense chromosomes of this organism encode approximately 12,500 predicted proteins, a high proportion of which have long, repetitive amino acid tracts. There are many genes for polyketide synthases and ABC transporters, suggesting an extensive secondary metabolism for producing and exporting small molecules. The genome is rich in complex repeats, one class of which is clustered and may serve as centromeres. Partial copies of the extrachromosomal ribosomal DNA (rDNA) element are found at the ends of each chromosome, suggesting a novel telomere structure and the use of a common mechanism to maintain both the rDNA and chromosomal termini. A proteome-based phylogeny shows that the amoebozoa diverged from the animal-fungal lineage after the plant-animal split, but Dictyostelium seems to have retained more of the diversity of the ancestral genome than have plants, animals or fungi.

1,289 citations


"Between a Pod and a Hard Test: The ..." refers background or methods in this paper

  • ...Amoebozoa is morphologically and ecologically very diverse including important pathogens to metazoans (e.g., Entamoeba and Acanthamoeba; Visvesvara et al. 2007) and the model organisms Dictyostelium discoideum and Physarum polycephalum (Eichinger et al. 2005; Schaap et al. 2015)....

    [...]

  • ...2007) and the model organisms Dictyostelium discoideum and Physarum polycephalum (Eichinger et al. 2005; Schaap et al. 2015)....

    [...]

Related Papers (5)