The genome of earliest animal with “elementary brain”

UMass Chan Medical School (UMMS) researchers, University of Florida (UF) researchers, and their collaborators sequenced the genome of, probably, the earliest animal with a complex nervous system.

The draft genome sequence of the sea animal known colloquially as the “sea gooseberry,” (Pleurobrachia bachei) and the paper entitled “The ctenophore genome and the evolutionary origins of neural systems” were both published online in Nature by an international team, which included corresponding lead authors from the University of Florida (L. L. Moroz and A. B. Kohn) and UMass Chan Medical School (E.I. Rogaev), as well as researchers from the Auburn University, University of Illinois Urbana-Champaign, Genetic Information Research Institute, USA; Academy of Sciences in Russia; Centre for Genomic Regulation and Universitat Pompeu Fabra in Spain; University of Groningen Medical Center, the Netherlands; University of Toronto, Canada; University of London, UK, and others. Ellen Kittler and Deep Sequencing Core at UMMS also participated in this study.

The Pleurobrachia bachei is one of approximately 150 species representing the group of pre-bilaterian animals known as comb jellies (Cternophore). This group of metazoans possesses both complex nervous and mesoderm-derived muscular systems.

The ultra-deep sequencing by Illumina platforms provided >700-fold coverage of Pleurobrachia’s genome. At least 19,523 predicted protein-coding genes and more than 300 families of transposable elements (8.5% of the genome) were found.  By the evolutionary analysis of Pleurobrachia genome and genes from different Ctenophore species and other animal lineages, the researchers suggested that Ctenophore can be placed as the earliest lineage within Metazoa. The hypothesis is supported by a comparative analysis of multiple gene families, metabolic and physiological data, and a study of transcriptomes from 10 Ctenophore species.

The research team further discovered that the ctenophore’s neural system, along with muscle specifications, likely has an independent origin from similar systems found in other animals. They found, to their surprise, a lack of classical neurotransmitters (apart from glutamate) and a number of genes essential for neural cell fate and differentiation in Pleurobrachia, despite the presence of a well-organized neural system or even an “elementary brain.” Ultrasensitive metabolic analysis, performed by the University of Florida group, revealed that ctenophores likely do not use serotonin, acetylcholine, dopamine, and many other common neurotransmitters as intercellular messengers. However, L-glutamate was predicted as a candidate neuromuscular transmitter in Pleurobrachia. The prediction was supported by unprecedented diversity of genes for ionotropic glutamate receptors (iGluRs) found in Pleurobrachia.

Evgeny Rogaev, Professor of Psychiatry at UMMS, whose laboratory performed the whole genome sequencing of Pleurobrachia, indicated a surprising finding that no canonical miRNAs and some genes essential for miRNA production were found. miRNA is the class of regulatory RNA that is thought to be essential for function and development in all animals.  Among the genes for small RNA processing enzymes, Pleurobrachia has Dicer, Ago, Piwi, and Hen1, but lacks Drosha, Pasha, and TRBP2 genes.  There are uncharacterized small RNAs in the Ctenophore species that may potentially have regulatory functions. The importance of posttranscriptional modifications in the diversity of RNA molecules in Pleurobrachia is illuminated by an extremely high number of genes for RNA-editing enzymes and RNA-binding proteins.  Dr. Rogaev comments that the independent origin and evolution of different nervous systems (NSs) is quite unexpected, but evolution of nervous systems towards complexity can be observed in different branches of diverged invertebrate and vertebrate animal lineages. The further study of the molecular mechanisms underlying the parallel evolution of the nervous system and the brain is an exciting research topic.

Moroz L. et al. The ctenophore genome and the evolutionary origins of neural systems. Nature, 2014, V.510, 109-114. http://www.nature.com/nature/journal/vaop/ncurrent/full/nature13400.html

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Correspondence and requests for materials should be addressed to L.L.M. (moroz@whitney.ufl.edu) or E.I.R. Evgeny.Rogaev@umassmed.edu) or A.B.K. (abkohn@msn.com)