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2015 Annual Science Report

Massachusetts Institute of Technology Reporting  |  JAN 2015 – DEC 2015

Early Animals: Sensory Systems and Combinatorial Codes

Project Summary

Understanding the evolution of integrated sensory organs—such as the eyes, ears and nose that develop in concert on our heads—is fundamental to understanding animal complexity. These are the features that permit movement and the environmental responses that characterize animals. We examine understudied early branches of the animal family tree, with a focus on the jellyfish Aurelia, to understand how the genetic regulation of sensory organs is conserved in some cases and evolves in others. Comparison of developmental regulation reveals how similar gene networks can be differentially modified and deployed, permitting the evolution of complex sensory systems. Jellyfish provide an ideal study system for the examination of the evolution of such sensory systems in animal evolution, as they are the most basal branch of the animal tree with multiple sensory modes, and these develop at multiple stages in a complex life history. This provides us the ability to compare and contrast within the broader cnidarian group to which jellyfish belong, and to the bilaterians, the broad group containing humans and most other animals. The application of genomic methods greatly enhances our ability to pursue these questions.

4 Institutions
3 Teams
2 Publications
0 Field Sites
Field Sites

Project Progress

Aurelia, the moon jellyfish provides an excellent model for the evolution of complex sensory systems. It possesses multiple sense organs that operate in different sensory modalities in a complex life history. Cnidaria are the most basal taxon with this complex repertoire of sense organs, and they exhibit evolutionary gain and loss of these sensory structures within the group. They also provide a valuable comparison to their sister clade, the Bilateria.

This year we published results on the combinatorial code of gene expression in sense organs using expression data from in situ hybridization and transcriptomes looking at candidate genes (Nakanishi et al. 2015). We then presented initial results of a more comprehensive analysis of transcriptomic data at the inaugural meeting of The Pan American Society for Evolutionary Developmental Biology.

Figure 1. Gene Network Analyses of stage specific RNA Seq data and Homeodomain Gene Function Associations. Differentially expressed genes were determined using EdgeR, with 2-3 biological replicates per life stage. The gene counts were normalized into Fragments Per Kilobase of transcript per Million mapped reads (FPKM), which were then averaged by life stage. The FPKM values for each gene were percent transformed, and then hierarchically clustered using Pearson correlation. Groups were chosen based on similar expression patterns, and are individually colored in the tree.
Figure 1. Gene Network Analyses of stage specific RNA Seq data and Homeodomain Gene Function Associations. Differentially expressed genes were determined using EdgeR, with 2-3 biological replicates per life stage. The gene counts were normalized into Fragments Per Kilobase of transcript per Million mapped reads (FPKM), which were then averaged by life stage. The FPKM values for each gene were percent transformed, and then hierarchically clustered using Pearson correlation. Groups were chosen based on similar expression patterns, and are individually colored in the tree. Several of these clades were analyzed using Genemania, using an iterative process. Aurelia genes from the clusters were submitted as human or fruit fly gene lists, with names based on each gene’s best BLAST match (e-value cutoff 1e-5). Following network analysis, the analysis was re-run, restricted to Homeodomain-containing genes and their associated genes. Functional enrichment of this restricted network was predicted in Genemania using an FDR cutoff of 0.05.008.

There are different tentacle types in the medusa and polyp life history stages in Aurelia. These are effectively sensory organs, but also engaged in motor response to sensation. They provide an opportunity to further study how genetic regulatory processes differentiate a suite of complicated structures. Preparatory to such studies, we characterized the differences between these tentacles of Aurelia using confocal and electron microscopy (Gold et al. 2015) and found structural evidence of a previously unrecognized motor apparatus involved in extension of the polyp tentacles, in addition to the already known mechanisms for tentacle contraction.

Fig 2. Morphology of the polyp oral tentacle in Aurelia sp.1. All scale bars represent 50 μm. (A) Longitudinal section of tentacle, revealing the morphology and distribution of ectodermal (ec) and endodermal (en) cells. (B) A similar image showing the distribution of nuclei in the tentacle. Note the row of large, vacuolated cells in the endoderm. (C) Longitudinal section demonstrating how anti-Ttub can be used to identify cnidocytes. Examples where enlarged cells (caused by the presence of the cnidocyte capsule) are co-localized with crescent-shaped nuclei are labeled with arrows. (D) Phalloidin staining at the base of a tentacle. (E) A partial stack of confocal images, revealing the circumferential myofibrils (Cm) underneath the longitudinal musculature of the epitheliomuscular cells. (F) Circumfirential fibers in E, along with electron microscopy not shown document circumferential contration and a previously unrecognized extensional motor apparatus.
Fig 2. Morphology of the polyp oral tentacle in Aurelia sp.1. All scale bars represent 50 μm. (A) Longitudinal section of tentacle, revealing the morphology and distribution of ectodermal (ec) and endodermal (en) cells. (B) A similar image showing the distribution of nuclei in the tentacle. Note the row of large, vacuolated cells in the endoderm. (C) Longitudinal section demonstrating how anti-Ttub can be used to identify cnidocytes. Examples where enlarged cells (caused by the presence of the cnidocyte capsule) are co-localized with crescent-shaped nuclei are labeled with arrows. (D) Phalloidin staining at the base of a tentacle. (E) A partial stack of confocal images, revealing the circumferential myofibrils (Cm) underneath the longitudinal musculature of the epitheliomuscular cells. (F) Circumfirential fibers in E, along with electron microscopy not shown document circumferential contration and a previously unrecognized extensional motor apparatus.

Publications

  • Gold, D. A., Nakanishi, N., Hensley, N. M., Cozzolino, K., Tabatabaee, M., Martin, M., … Jacobs, D. K. (2015). Structural and Developmental Disparity in the Tentacles of the Moon Jellyfish Aurelia sp.1. PLoS ONE, 10(8), e0134741. doi:10.1371/journal.pone.0134741

  • Nakanishi, N., Camara, A. C., Yuan, D. C., Gold, D. A., & Jacobs, D. K. (2015). Gene Expression Data from the Moon Jelly, Aurelia, Provide Insights into the Evolution of the Combinatorial Code Controlling Animal Sense Organ Development. PLoS ONE, 10(7), e0132544. doi:10.1371/journal.pone.0132544