Unknown,Transcriptomics,Genomics,Proteomics

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Bacterial discrimination by Dictyostelid amoebae reveals the complexity of ancient interspecies interactions

ABSTRACT: Transcriptional profiling of D. discoideum revealed sets of genes whose expression is enriched in amoebae interacting with different species of bacteria, including sets that appear specific to amoebae interacting with Gram(+), or with Gram(-) bacteria. In a genetic screen utilizing the growth of mutant amoebae on a variety of bacteria as a phenotypic readout, we identified amoebal genes that are only required for growth on Gram(+) bacteria, including one that encodes the cell surface protein gp130, as well as several genes that are only required for growth on Gram(-) bacteria including one that encodes a putative lysozyme, AlyL. These genes are required for parts of the transcriptional response of wild-type amoebae, and this allowed their classification into potential response pathways. Transcriptional profiling of amoebal response to different bacteria.

ORGANISM(S): Dictyostelium discoideum

SUBMITTER: Balaji Santhanam

PROVIDER: E-GEOD-46386 | biostudies-arrayexpress |

REPOSITORIES: biostudies-arrayexpress

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Bacterial discrimination by dictyostelid amoebae reveals the complexity of ancient interspecies interactions.

Nasser Waleed W Santhanam Balaji B Miranda Edward Roshan ER Parikh Anup A Juneja Kavina K Rot Gregor G Dinh Chris C Chen Rui R Zupan Blaz B Shaulsky Gad G Kuspa Adam A

Current biology : CB 20130509 10

<h4>Background</h4>Amoebae and bacteria interact within predator-prey and host-pathogen relationships, but the general response of amoeba to bacteria is not well understood. The amoeba Dictyostelium discoideum feeds on, and is colonized by, diverse bacterial species, including Gram-positive [Gram(+)] and Gram-negative [Gram(-)] bacteria, two major groups of bacteria that differ in structure and macromolecular composition.<h4>Results</h4>Transcriptional profiling of D. discoideum revealed sets of ...[more]

PMID: 23664307

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Project description:Development of the soil amoeba Dictyostelium discoideum is triggered by starvation. When placed on a solid substrate, the starving solitary amoebae cease growth, communicate via extracellular cAMP, aggregate by tens of thousands and develop into fully integrated multicellular organisms. Early phases of the developmental program are often studied in cells starved in suspension while cAMP is provided exogenously. Previous studies revealed massive shifts in the transcriptome under these developmental conditions and a close relationship between gene expression and morphogenesis, but were limited by the sampling frequency and the resolution of the methods. Here, we combine the superior depth and specificity of RNA-seq with high frequency sampling during filter development and cAMP pulsing in suspension. We found that the developmental transcriptome exhibits mostly gradual changes interspersed by a few instances of large changes. Considering the whole transcriptome as a single phenotype, we treated each time point as an independent entity and were able to characterize development as groups of similar time points separated by gaps. The grouped time points represent gradual changes in mRNA abundance and the gaps represent times during which many genes are differentially expressed rapidly. Comparing development on solid substrate to development in suspension revealed that gene expression in filter developed cells lagged behind cells treated with exogenous cAMP in suspension. The high sampling frequency revealed many genes whose regulation is reproducibly more complex than indicated by previous studies. Gene Ontology enrichment analysis showed that the transition to multicellularity at the mound stage coincided with rapid accumulation of transcripts associated with mitosis and DNA replicative processes. Later development included the up-regulation of organic signaling molecules and co-factor biosynthesis. We observed multiple instances of enrichment of oxidation-reduction and reactive oxygen related terms. Our analysis also demonstrated a high level of synchrony between the developing structures throughout development. Our data describe D. discoideum development as a series of coordinated cellular and multicellular activities. Coordination occurred within fields of aggregating cells and between multicellular bodies, such as mounds or migratory slugs that experience both cell-cell contact and various soluble signaling regimes. These time courses, sampled at the highest temporal resolution to date in this system, provide a comprehensive resource for future studies of developmental gene expression. Dictyosteloium discoideum gene expression (mRNA) profiles from two experimental time courses: development on filters and cAMP signaling in suspension. Filter development consists of 2 replicates of 19 time point samples, while cAMP in suspension contains 3 replicates of 10, 10 and 9 samples each.

Dataset Information

Bacterial discrimination by Dictyostelid amoebae reveals the complexity of ancient interspecies interactions

Publications

Bacterial discrimination by dictyostelid amoebae reveals the complexity of ancient interspecies interactions.

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