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Origin and evolution of the slime molds (Mycetozoa)

ABSTRACT: The Mycetozoa include the cellular (dictyostelid), acellular (myxogastrid), and protostelid slime molds. However, available molecular data are in disagreement on both the monophyly and phylogenetic position of the group. Ribosomal RNA trees show the myxogastrid and dictyostelid slime molds as unrelated early branching lineages, but actin and beta-tubulin trees place them together as a single coherent (monophyletic) group, closely related to the animal-fungal clade. We have sequenced the elongation factor-1alpha genes from one member of each division of the Mycetozoa, including Dictyostelium discoideum, for which cDNA sequences were previously available. Phylogenetic analyses of these sequences strongly support a monophyletic Mycetozoa, with the myxogastrid and dictyostelid slime molds most closely related to each other. All phylogenetic methods used also place this coherent Mycetozoan assemblage as emerging among the multicellular eukaryotes, tentatively supported as more closely related to animals + fungi than are green plants. With our data there are now three proteins that consistently support a monophyletic Mycetozoa and at least four that place these taxa within the "crown" of the eukaryote tree. We suggest that ribosomal RNA data should be more closely examined with regard to these questions, and we emphasize the importance of developing multiple sequence data sets.

SUBMITTER: Baldauf SL

PROVIDER: S-EPMC23686 | biostudies-literature | 1997 Oct

REPOSITORIES: biostudies-literature

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Origin and evolution of the slime molds (Mycetozoa)

Baldauf S L SL Doolittle W F WF

Proceedings of the National Academy of Sciences of the United States of America 19971001 22

The Mycetozoa include the cellular (dictyostelid), acellular (myxogastrid), and protostelid slime molds. However, available molecular data are in disagreement on both the monophyly and phylogenetic position of the group. Ribosomal RNA trees show the myxogastrid and dictyostelid slime molds as unrelated early branching lineages, but actin and beta-tubulin trees place them together as a single coherent (monophyletic) group, closely related to the animal-fungal clade. We have sequenced the elongati ...[more]

PMID: 9342353

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Project description:BackgroundMulticellularity in cellular slime molds is achieved by aggregation of several hundreds to thousands of cells. In the model slime mold Dictyostelium discoideum, adenosine is known to increase the aggregate size and its antagonist caffeine reduces the aggregate size. However, it is not clear if the actions of adenosine and caffeine are evolutionarily conserved among other slime molds known to use structurally unrelated chemoattractants. We have examined how the known factors affecting aggregate size are modulated by adenosine and caffeine.ResultAdenosine and caffeine induced the formation of large and small aggregates respectively, in evolutionarily distinct slime molds known to use diverse chemoattractants for their aggregation. Due to its genetic tractability, we chose D. discoideum to further investigate the factors affecting aggregate size. The changes in aggregate size are caused by the effect of the compounds on several parameters such as cell number and size, cell-cell adhesion, cAMP signal relay and cell counting mechanisms. While some of the effects of these two compounds are opposite to each other, interestingly, both compounds increase the intracellular glucose level and strengthen cell-cell adhesion. These compounds also inhibit the synthesis of cAMP phosphodiesterase (PdsA), weakening the relay of extracellular cAMP signal. Adenosine as well as caffeine rescue mutants impaired in stream formation (pde4- and pdiA-) and colony size (smlA- and ctnA-) and restore their parental aggregate size.ConclusionAdenosine increased the cell division timings thereby making large number of cells available for aggregation and also it marginally increased the cell size contributing to large aggregate size. Reduced cell division rates and decreased cell size in the presence of caffeine makes the aggregates smaller than controls. Both the compounds altered the speed of the chemotactic amoebae causing a variation in aggregate size. Our data strongly suggests that cytosolic glucose and extracellular cAMP levels are the other major determinants regulating aggregate size and pattern. Importantly, the aggregation process is conserved among different lineages of cellular slime molds despite using unrelated signalling molecules for aggregation.

Project description:Amoebae that make fruiting bodies consisting of a stalk and spores and classified as closely related to the myxogastrids have classically been placed in the taxon Eumycetozoa. Traditionally, there are three groups comprising Eumycetozoa: myxogastrids, dictyostelids, and the so-called protostelids. Dictyostelids and myxogastrids both make multicellular fruiting bodies that may contain hundreds of spores. Protostelids are those amoebae that make simple fruiting bodies consisting of a stalk and one or a few spores. Protostelid-like organisms have been suggested as the progenitors of the myxogastrids and dictyostelids, and they have been used to formulate hypotheses on the evolution of fruiting within the group. Molecular phylogenies have been published for both myxogastrids and dictyostelids, but little molecular phylogenetic work has been done on the protostelids. Here we provide phylogenetic trees based on the small subunit ribosomal RNA gene (SSU) that include 21 protostelids along with publicly available sequences from a wide variety of amoebae and other eukaryotes. SSU trees recover seven well supported clades that contain protostelids but do not appear to be specifically related to one another and are often interspersed among established groups of amoebae that have never been reported to fruit. In fact, we show that at least two taxa unambiguously belong to amoebozoan lineages where fruiting has never been reported. These analyses indicate that we can reject a monophyletic Eumycetozoa, s.l. For this reason, we will hereafter refer to those slime molds with simple fruiting as protosteloid amoebae and/or protosteloid slime molds, not as protostelids. These results add to our understanding of amoebozoan biodiversity, and demonstrate that the paradigms for understanding both nonfruiting and sporulating amoebae must be integrated. Finally, we suggest strategies for future research on protosteloid amoebae and nonfruiting amoebae, and discuss the impact of this work for taxonomists and phylogenomicists.

Dataset Information

Origin and evolution of the slime molds (Mycetozoa)

Publications

Origin and evolution of the slime molds (Mycetozoa)

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