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Statistical image analysis reveals features affecting fates of Myxococcus xanthus developmental aggregates.

ABSTRACT: Starving Myxococcus xanthus bacteria use their motility systems to self-organize into multicellular fruiting bodies, large mounds in which cells differentiate into metabolically inert spores. Despite the identification of the genetic pathways required for aggregation and the use of microcinematography to observe aggregation dynamics in WT and mutant strains, a mechanistic understanding of aggregation is still incomplete. For example, it is not clear why some of the initial aggregates mature into fruiting bodies, whereas others disperse, merge, or split into two. Here, we develop high-throughput image quantification and statistical analysis methods to gain insight into M. xanthus developmental aggregation dynamics. A quantitative metric of features characterizing each aggregate is used to deduce the properties of the aggregates that are correlated with each fate. The analysis shows that small aggregate size but not neighbor-related parameters correlate with aggregate dispersal. Furthermore, close proximity is necessary but not sufficient for aggregate merging. Finally, splitting occurs for those aggregates that are unusually large and elongated. These observations place severe constraints on the underlying aggregation mechanisms and present strong evidence against the role of long-range morphogenic gradients or biased cell exchange in the dispersal, merging, or splitting of transient aggregates. This approach can be expanded and adapted to study self-organization in other cellular systems.

SUBMITTER: Xie C

PROVIDER: S-EPMC3078403 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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Statistical image analysis reveals features affecting fates of Myxococcus xanthus developmental aggregates.

Xie Chunyan C Zhang Haiyang H Shimkets Lawrence J LJ Igoshin Oleg A OA

Proceedings of the National Academy of Sciences of the United States of America 20110321 14

Starving Myxococcus xanthus bacteria use their motility systems to self-organize into multicellular fruiting bodies, large mounds in which cells differentiate into metabolically inert spores. Despite the identification of the genetic pathways required for aggregation and the use of microcinematography to observe aggregation dynamics in WT and mutant strains, a mechanistic understanding of aggregation is still incomplete. For example, it is not clear why some of the initial aggregates mature into ...[more]

PMID: 21436028

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Project description:BackgroundThe Myxococcales are well known for their predatory and developmental social processes, and for the molecular complexity of regulation of these processes. Many species within this order have unusually large genomes compared to other bacteria, and their genomes have many genes that are unique to one specific sequenced species or strain. Here, we describe RNAseq based transcriptome analysis of the FruA regulon of Myxococcus xanthus and a comparative RNAseq analysis of two Myxococcus species, M. xanthus and Myxococcus stipitatus, as they respond to starvation and begin forming fruiting bodies.ResultsWe show that both species have large numbers of genes that are developmentally regulated, with over half the genome showing statistically significant changes in expression during development in each species. We also included a non-fruiting mutant of M. xanthus that is missing the transcriptional regulator FruA to identify the direct and indirect FruA regulon and to identify transcriptional changes that are specific to fruiting and not just the starvation response. We then identified Interpro gene ontologies and COG annotations that are significantly up- or down-regulated during development in each species. Our analyses support previous data for M. xanthus showing developmental upregulation of signal transduction genes, and downregulation of genes related to cell-cycle, translation, metabolism, and in some cases, DNA replication. Gene expression in M. stipitatus follows similar trends. Although not all specific genes show similar regulation patterns in both species, many critical developmental genes in M. xanthus have conserved expression patterns in M. stipitatus, and some groups of otherwise unstudied orthologous genes share expression patterns.ConclusionsBy identifying the FruA regulon and identifying genes that are similarly and uniquely regulated in two different species, this work provides a more complete picture of transcription during Myxococcus development. We also provide an R script to allow other scientists to mine our data for genes whose expression patterns match a user-selected gene of interest.

Project description:Myxococcus xanthus is a gram-negative bacterium which has a complex life cycle. Autochemotaxis, a process whereby cells release a self-generated signaling molecule, may be the principal mechanism facilitating directed motility in both the vegetative swarming and developmental aggregation stages of this life cycle. The process requires the Frz signal transduction system, including FrzZ, a protein which is composed of two domains, both showing homology to the enteric chemotaxis response regulator CheY. The first domain of FrzZ (FrzZ1), when expressed as bait in the yeast two-hybrid system and screened against a library, was shown to potentially interact with the C-terminal portion of a protein encoding an ATP-binding cassette (AbcA). The activation domain-AbcA fusion protein did not interact with the second domain of FrzZ (FrzZ2) or with two other M. xanthus response regulator-containing proteins presented as bait, suggesting that the FrzZ1-AbcA interaction may be specific. Cloning and sequencing of the upstream region of the abcA gene showed the ATP-binding cassette to be linked to a large hydrophobic, potentially membrane-spanning domain. This domain organization is characteristic of a subgroup of ABC transporters which perform export functions. Cloning and sequencing downstream of abcA indicated that the ABC transporter is at the start of an operon containing three open reading frames. An insertion mutation in the abcA gene resulted in cells displaying the frizzy aggregation phenotype, providing additional evidence that FrzZ and AbcA may be part of the same signal transduction pathway. Cells with mutations in genes downstream of abcA showed no developmental defects. Analysis of the proposed exporter role of AbcA in cell mixing experiments showed that the ABC transporter mutant could be rescued by extracellular complementation. We speculate that the AbcA protein may be involved in the export of a molecule required for the autochemotactic process.

Dataset Information

Statistical image analysis reveals features affecting fates of Myxococcus xanthus developmental aggregates.

Publications

Statistical image analysis reveals features affecting fates of Myxococcus xanthus developmental aggregates.

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