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

. 2017 Sep 01 ; 34 (9) : 2258-2270.

Language English Country United States Media print

Document type Journal Article, Research Support, U.S. Gov't, Non-P.H.S., Research Support, Non-U.S. Gov't

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.

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Adl SM, Simpson AG, Lane CE, Lukes J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, et al.2012. The revised classification of eukaryotes. J Eukaryot Microbiol. 59:429–493. PubMed PMC

Amaral Zettler LA, Nerad TA, O’Kelly CJ, Peglar MT, Gillevet PM, Silberman JD, Sogin ML.. 2000. A molecular reassessment of the Leptomyxid amoebae. Protist 151:275–282. PubMed

Berney C, Geisen S, Van Wichelen J, Nitsche F, Vanormelingen P, Bonkowski M, Bass D.. 2015. Expansion of the ‘reticulosphere’: diversity of novel branching and network-forming amoebae helps to define Variosea (Amoebozoa). Protist 166:271–295. PubMed

Bolivar I, Fahrni JF, Smirnov AV, Pawlowski J.. 2001. SSU rRNA-based phylogenetic position of the genera Amoeba and Chaos (Lobosea, Gymnamoebia): the origin of gymnamoebae revisited. Mol Biol Evol. 18:2306–2314. PubMed

Brown MW, Sharpe SC, Silberman JD, Heiss AA, Lang BF, Simpson AGB, Roger AJ.. 2013. Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc R Soc B: Biol Sci. 280:20131755–20131755. PubMed PMC

Brown MW, Silberman JD.. 2013. The non-dictyostelid sorocarpic amoebae. In Romeralo, Escalante, Baldauf, editors. Dictyostelids – evolution, genomics and cell biology. Heidelberg (Germany: ): Springer; pp 219–242.

Brown MW, Silberman JD, Spiegel FW.. 2011. “Slime molds” among the Tubulinea (Amoebozoa): molecular systematics and taxonomy of Copromyxa. Protist 162:277–287. PubMed

Brown MW, Spiegel FW, Silberman JD.. 2007. Amoeba at attention: phylogenetic affinity of Sappinia pedata. J Eukaryot Microbiol. 54:511–519. PubMed

Cavalier-Smith T. 1998. A revised six-kingdom system of life. Biol Rev Camb Philos Soc. 73:203–266. PubMed

Cavalier-Smith T, Chao EE, Lewis R.. 2016. 187-Gene phylogeny of protozoan phylum Amoebozoa reveals a new class (Cutosea) of deep-branching, ultrastructurally unique, enveloped marine Lobosa and clarifies amoeba evolution. Mol Phylogenet Evol. 99:275–296. PubMed

Cavalier-Smith T, Chao EEY, Oates B.. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. Eur J Protistol. 40:21–48.

Cavalier-Smith T, Fiore-Donno AM, Chao E, Kudryavtsev A, Berney C, Snell EA, Lewis R.. 2015. Multigene phylogeny resolves deep branching of Amoebozoa. Mol Phylogenet Evol. 83:293–304. PubMed

Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, et al.2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57. PubMed PMC

Eme L, Sharpe SC, Brown MW, Roger AJ.. 2014. On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb Perspect Biol. 6: PubMed PMC

Fahrni JF, Bolivar I, Berney C, Nassanova E, Smirnov AV, Pawlowski J.. 2003. Phylogeny of lobose amoebae based on actin and small-subunit ribosomal RNA genes. Mol Biol Evol. 20:1881–1886. PubMed

Fiore-Donno AM, Nikolaev SI, Nelson M, Pawlowski J, Cavalier-Smith T, Baldauf SL.. 2010. Deep phylogeny and evolution of slime moulds (mycetozoa). Protist 161:55–70. PubMed

Goodenough U, Heitman J.. 2014. Origins of eukaryotic sexual reproduction. Cold Spring Harb Perspect Biol. 6:a016154–a016154. PubMed PMC

Jeffroy O, Brinkmann H, Delsuc F, Philippe H.. 2006. Phylogenomics: the beginning of incongruence? Trends Genet. 22:225–231. PubMed

Kudryavtsev A, Brown MW, Tice A, Spiegel FW, Pawlowski J, Anderson OR.. 2014. A revision of the order pellitida Smirnov et al., 2011 (Amoebozoa, Discosea) based on ultrastructural and molecular evidence, with description of Endostelium crystalliferum n. sp. Protist 165:208–229. PubMed

Kudryavtsev A, Pawlowski J.. 2013. Squamamoeba japonica n. g. n. sp. (Amoebozoa): a deep-sea amoeba from the Sea of Japan with a novel cell coat structure. Protist 164:13–23. PubMed

Lahr DJ, Grant J, Molestina R, Katz LA, Anderson OR.. 2015. Sapocribrum chincoteaguense n. gen. n. sp.: a small, scale-bearing Amoebozoan with Flabellinid affinities. J Eukaryot Microbiol. 62:444–453. PubMed PMC

Lahr DJ, Grant J, Nguyen T, Lin JH, Katz LA.. 2011a. Comprehensive phylogenetic reconstruction of amoebozoa based on concatenated analyses of SSU-rDNA and actin genes. PLoS ONE. 6:e22780.. PubMed PMC

Lahr DJG, Parfrey LW, Mitchell EAD, Katz LA, Lara E.. 2011b. The chastity of amoebae: re-evaluating evidence for sex in amoeboid organisms. Proc R Soc B: Biol Sci. 278:2081–2090. PubMed PMC

Lahr DJ, Grant JR, Katz LA.. 2013. Multigene phylogenetic reconstruction of the Tubulinea (Amoebozoa) corroborates four of the six major lineages, while additionally revealing that shell composition does not predict phylogeny in the Arcellinida. Protist 164:323–339. PubMed

Lartillot N, Philippe H.. 2008. Improvement of molecular phylogenetic inference and the phylogeny of Bilateria. Philos Trans R Soc Lond B Biol Sci. 363:1463–1472. PubMed PMC

Lartillot N, Rodrigue N, Stubbs D, Richer J.. 2013. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst Biol. 62:611–615. PubMed

Le SQ, Gascuel O.. 2008. An improved general amino acid replacement matrix. Mol Biol Evol. 25:1307–1320. PubMed

Martin GW, Alexopoulos CJ.. 1969. Monograph of the Myxomycetes. Iowa City (IA: ): University of Iowa Press.

Mikrjukov KA, Mylnikov AP.. 1998. The fine structure of a carnivorous multiflagellar protist Multicilia marina Cienkowski, 1881 (flagellata incertae sedis). Eur J Protistol. 34:391–401.

Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ.. 2014. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 32:268–274. PubMed PMC

Nikolaev SI, Berney C, Petrov NB, Mylnikov AP, Fahrni JF, Pawlowski J.. 2006. Phylogenetic position of Multicilia marina and the evolution of Amoebozoa. Int J Syst Evol Microbiol. 56:1449–1458. PubMed

Olive LS. 1975. The mycetozoans. New York, NY: Academic Press.

Olive LS, Bennett WE, Deasey MC.. 1984. The new protostelid genus Endostelium. Mycologia 76:884.

Olsen GJ. 1987. Earliest phylogenetic branchings: comparing rRNA-based evolutionary trees inferred with various techniques. Cold Spring Harb Symp Quant Biol. 52:825–837. PubMed

Page FC. 1976. A revised classification of the Gymnamoebia (Protozoa: Sarcodina). Zool J Linnean Soc. 58:61–77.

Page FC. 1983. Marine gymnamoebae. Cambridge: Institute of Terrestrial Ecology, Culture Centre of Algae and Protozoa.

Page FC. 1988. A new key to freshwater and soil gymnamoebae. Ambleside, Cumbria (United Kingdom: ): Freshwater Biological Association.

Pánek T, Zadrobílková E, Walker G, Brown MW, Gentekaki E, Hroudová M, Kang S, Roger AJ, Tice AK, Vlček C, et al.2016. First multigene analysis of Archamoebae (Amoebozoa: Conosa) robustly reveals its phylogeny and shows that Entamoebidae represents a deep lineage of the group. Mol Phylogenet Evol. 98:41–51. PubMed

Patterson DJ. 1999. The diversity of eukaryotes. Am Nat. 154:S96–S124. PubMed

Pawlowski J. 2008. The twilight of Sarcodina: a molecular perspective on the polyphyletic origin of amoeboid protists. Protistology 5:281–302.

Ptackova E, Kostygov AY, Chistyakova LV, Falteisek L, Frolov AO, Patterson DJ, Walker G, Cepicka I.. 2013. Evolution of Archamoebae: morphological and molecular evidence for pelobionts including Rhizomastix, Entamoeba, Iodamoeba, and Endolimax. Protist 164:380–410. PubMed

Pussard M. 1973. Description d'une amibe de type flabellulien, Pessonella marginata n.g. n. sp. (Mayorellidae, amoebaea). Protistologica 9:175–185.

Reinhardt DJ. 1968. Development of the mycetozoan Echinosteliopsis oligospora. J Protozool. 15:480–493. PubMed

Romeralo M, Skiba A, Gonzalez-Voyer A, Schilde C, Lawal H, Kedziora S, Cavender JC, Glockner G, Urushihara H, Schaap P.. 2013. Analysis of phenotypic evolution in Dictyostelia highlights developmental plasticity as a likely consequence of colonial multicellularity. Proc Biol Sci. 280:20130976.. PubMed PMC

Schaap P, Barrantes I, Minx P, Sasaki N, Anderson RW, Benard M, Biggar KK, Buchler NE, Bundschuh R, Chen X, et al.2015. The Physarum polycephalum genome reveals extensive use of prokaryotic two-component and metazoan-type tyrosine kinase signaling. Genome Biol Evol. 8:109–125. PubMed PMC

Schmarda LK. 1871. Zoologie. W. Braumüller. Berlin, Germany.

Seravin LN, Goodkov AV.. 1987. The flagella of the freshwater amoeba Pelomyxa palustris. Tsitologiya 29:721–724.

Shadwick LL, Spiegel FW, Shadwick JD, Brown MW, Silberman JD.. 2009. Eumycetozoa = Amoebozoa?: SSUrDNA phylogeny of protosteloid slime molds and its significance for the amoebozoan supergroup. PLoS ONE. 4:e6754.. PubMed PMC

Shadwick LL, Brown MW, Tice AK, Spiegel FW.. 2016. A new amoeba with protosteloid fruiting: Luapeleamoeba hula n. g. n. sp. Acta Protozool. 55:123–134.

Shimodaira H. 2002. An approximately unbiased test of phylogenetic tree selection. Syst Biol. 51:492–508. PubMed

Smirnov AV, Nassonova E, Berney C, Fahrni J, Bolivar I, Pawlowski J.. 2005. Molecular phylogeny and classification of the lobose amoebae. Protist 156:129–142. PubMed

Smirnov AV, Chao E, Nassonova ES, Cavalier-Smith T.. 2011. A revised classification of naked lobose amoebae (Amoebozoa: obosa). Protist 162:545–570. PubMed

Spiegel FW. 1990. Phylum plasmodial slime molds, Class Protostelida In: Margulis JOC L., Melkonian M., Chapman D., editors. Handbook of Protoctista. Boston: Jones and Bartlett; pp. 484–497.

Spiegel FW. 1991. A proposed phylogeny of the flagellated protostelids. Biosystems 25:113–120. PubMed

Spiegel FW. 2011. Commentary on the chastity of amoebae: re-evaluating evidence for sex in amoeboid organisms. Proc R Soc B: Biol Sci. 278:2096–2097. PubMed PMC

Spiegel FW, Feldman J.. 1985. Obligate amoebae of the protostelids: significance for the concept of Eumycetozoa. Biosystems 18:377–386. PubMed

Spiegel FW, Feldman J.. 1989. Fruiting body development in the mycetozoan Echinostelium bisporum. Can J Bot. 67:1285–1293.

Spiegel FW, Feldman J.. 1993. Fruiting Body Ultrastructure in the Protostelid Schizoplasmodiopsis vulgare. Mycologia 85:894.

Spiegel FW, Lee SB, Rusk SA.. 1995. Eumycetozoans and molecular systematics. Can J Bot. 73:s738–s746.

Spiegel FW, Olive LS, Brown RM.. 1979. Roles of actin during sporocarp culmination in the simple mycetozoan Planoprotostelium aurantium. Proc Natl Acad Sci U S A. 76:2335–2339. PubMed PMC

Tekle YI, Grant J, Anderson OR, Nerad TA, Cole JC, Patterson DJ, Katz LA.. 2008. Phylogenetic placement of diverse amoebae inferred from multigene analyses and assessment of clade stability within ‘Amoebozoa’ upon removal of varying rate classes of SSU-rDNA. Mol Phylogenet Evol. 47:339–352. PubMed

Tekle YI, Anderson OR, Katz LA, Maurer-Alcala XX, Romero MA, Molestina R.. 2016. Phylogenomics of ‘Discosea’: a new molecular phylogenetic perspective on Amoebozoa with flat body forms. Mol Phylogenet Evol. 99:144–154. PubMed

Tekle YI, Wood FC, Katz LA, Ceron-Romero MA, Gorfu LA.. 2017. Amoebozoans are secretly but ancestrally sexual: evidence for sex genes and potential novel crossover pathways in diverse groups of amoebae. Genome Biol Evol doi:10.1093/gbe/evx002. PubMed PMC

Tice AK, Shadwick LL, Fiore-Donno AM, Geisen S, Kang S, Schuler GA, Spiegel FW, Wilkinson KA, Bonkowski M, Dumack K, et al.2016a. Expansion of the molecular and morphological diversity of Acanthamoebidae (Centramoebida, Amoebozoa) and identification of a novel life cycle type within the group. Biol Direct. 11:69.. PubMed PMC

Tice AK, Silberman JD, Walthall AC, Le KND, Spiegel FW, Brown MW.. 2016b. Sorodiplophrys stercorea: another novel lineage of sorocarpic multicellularity. J Eukaryot Microbiol. 63:623–628. PubMed

Visvesvara GS, Moura H, Schuster FL.. 2007. Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol Med Microbiol. 50:1–26. PubMed

Walker G, Simpson AGB, Edgcomb V, Sogin ML, Patterson DJ.. 2001. Ultrastructural identies of Mastigamoeba punctachora, Mastigamoeba simplex and Mastigella commutans and assessment of hypotheses of relatedness of the pelobionts (Protista). Eur J Protistol. 37:25–49.

Wang HC, Susko E, Roger AJ.. 2014. An amino acid substitution-selection model adjusts residue fitness to improve phylogenetic estimation. Mol Biol Evol. 31:779–792. PubMed

Whitney KD, Bennett WE, Olive LS.. 1982. Observations on Echinostelium bisporum. Mycologia 74:677–680.

Yubuki N, Leander BS.. 2013. Evolution of microtubule organizing centers across the tree of eukaryotes. Plant J. 75:230–244. PubMed

Zadrobilkova E, Walker G, Cepicka I.. 2015. Morphological and molecular evidence support a close relationship between the free-living archamoebae Mastigella and Pelomyxa. Protist 166: 14–41. PubMed

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