New genomes, new taxa and deep questions in the eukaryotic tree of life: a meeting report on the EMBO comparative genomics conference

A report on the meeting Comparative Genomics of Eukaryotic Microorganisms: understanding the complexity of diversity. Sant Feliu de Guíxols, Spain. October 15-20, 2011

Evolution of the MAGUK protein gene family in premetazoan lineages

<p>Abstract</p> <p>Background</p> <p>Cell-to-cell communication is a key process in multicellular organisms. In multicellular animals, scaffolding proteins belonging to the family of membrane-associated guanylate kinases (MAGUK) are involved in the regulation and formation of cell junctions. These MAGUK proteins were believed to be exclusive to Metazoa. However, a MAGUK gene was recently identified in an EST survey of <it>Capsaspora owczarzaki</it>, an unicellular organism that branches off near the metazoan clade. To further investigate the evolutionary history of MAGUK, we have undertook a broader search for this gene family using available genomic sequences of different opisthokont taxa.</p> <p>Results</p> <p>Our survey and phylogenetic analyses show that MAGUK proteins are present not only in Metazoa, but also in the choanoflagellate <it>Monosiga brevicollis </it>and in the protist <it>Capsaspora owczarzaki</it>. However, MAGUKs are absent from fungi, amoebozoans or any other eukaryote. The repertoire of MAGUKs in Placozoa and eumetazoan taxa (Cnidaria + Bilateria) is quite similar, except for one class that is missing in <it>Trichoplax</it>, while Porifera have a simpler MAGUK repertoire. However, Vertebrata have undergone several independent duplications and exhibit two exclusive MAGUK classes. Three different MAGUK types are found in both <it>M. brevicollis </it>and <it>C. owczarzaki: DLG, MPP and MAGI</it>. Furthermore, <it>M. brevicollis </it>has suffered a lineage-specific diversification.</p> <p>Conclusions</p> <p>The diversification of the MAGUK protein gene family occurred, most probably, prior to the divergence between Metazoa+choanoflagellates and the <it>Capsaspora</it>+<it>Ministeria </it>clade. A MAGI-like, a DLG-like, and a MPP-like ancestral genes were already present in the unicellular ancestor of Metazoa, and new gene members have been incorporated through metazoan evolution within two major periods, one before the sponge-eumetazoan split and another within the vertebrate lineage. Moreover, choanoflagellates have suffered an independent MAGUK diversification. This study highlights the importance of generating enough genome data from the broadest possible taxonomic sampling, in order to fully understand the evolutionary history of major protein gene families.</p

The Capsaspora genome reveals a complex unicellular prehistory of animals

Suga, Hiroshi et al.-- This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.To reconstruct the evolutionary origin of multicellular animals from their unicellular ancestors, the genome sequences of diverse unicellular relatives are essential. However, only the genome of the choanoflagellate Monosiga brevicollis has been reported to date. Here we completely sequence the genome of the filasterean Capsaspora owczarzaki, the closest known unicellular relative of metazoans besides choanoflagellates. Analyses of this genome alter our understanding of the molecular complexity of metazoans' unicellular ancestors showing that they had a richer repertoire of proteins involved in cell adhesion and transcriptional regulation than previously inferred only with the choanoflagellate genome. Some of these proteins were secondarily lost in choanoflagellates. In contrast, most intercellular signalling systems controlling development evolved later concomitant with the emergence of the first metazoans. We propose that the acquisition of these metazoan-specific developmental systems and the co-option of pre-existing genes drove the evolutionary transition from unicellular protists to metazoans. © 2013 Macmillan Publishers Limited. All rights reserved.H.S. was supported by the Marie Curie Intra-European Fellowship within the 7th European Community Framework Programme. Genome sequencing, assembly and some supporting analysis was supported by grants from the National Human Genome Research Institute (HG003067-05 through HG003067-10), as were C.N., C.R., B.H. and Z.C. B.F.L. and A.J.R. acknowledge financial support through the Canadian Research Chair program. This study was supported by an ICREA contract, a European Research Council Starting Grant (ERC-2007-StG-206883) and a grant (BFU2011-23434) from the Spanish Ministry of the Economy and Competitiveness (MINECO) awarded to I.R.-T. M.V. was supported by CNRS, the Agence Nationale de la Recherche (ANR grant BLAN-0294) and the Institut Universitaire de France.Peer Reviewe

A Broad Genomic Survey Reveals Multiple Origins and Frequent Losses in the Evolution of Respiratory Hemerythrins and Hemocyanins

Abstract Hemerythrins and hemocyanins are respiratory proteins present in some of the most ecologically diverse animal lineages; however, the precise evolutionary history of their enzymatic domains (hemerythrin, hemocyanin M, and tyrosinase) is still not well understood. We survey a wide dataset of prokaryote and eukaryote genomes and RNAseq data to reconstruct the phylogenetic origins of these proteins. We identify new species with hemerythrin, hemocyanin M, and tyrosinase domains in their genomes, particularly within animals, and demonstrate that the current distribution of respiratory proteins is due to several events of lateral gene transfer and/or massive gene loss. We conclude that the last common metazoan ancestor had at least two hemerythrin domains, one hemocyanin M domain, and six tyrosinase domains. The patchy distribution of these proteins among animal lineages can be partially explained by physiological adaptations, making these genes good targets for investigations into the interplay between genomic evolution and physiological constraints

The evolution of the GPCR signaling system in eukaryotes: Modularity, conservation, and the transition to metazoan multicellularity

The G-protein-coupled receptor (GPCR) signaling system is one of themain signaling pathways in eukaryotes. Here, we analyze the evolutionary history of all its components, from receptors to regulators, to gain a broad picture of its system-level evolution. Using eukaryotic genomes covering most lineages sampled to date, we find that the various components of the GPCR signaling pathway evolved independently, highlighting the modular nature of this system. Our data show that some GPCR families, G proteins, and regulators of G proteins diversified through lineage-specific diversifications and recurrent domain shuffling. Moreover, most of the gene families involved in the GPCR signaling system were already present in the last common ancestor of eukaryotes. Furthermore, we show that the unicellular ancestor of Metazoa already had most of the cytoplasmic components of the GPCR signaling system, including, remarkably, all the G protein alpha subunits, which are typical of metazoans. Thus, we show how the transition to multicellularity involved conservation of the signaling transduction machinery, as well as a burst of receptor diversification to cope with the new multicellular necessities. © The Author(s) 2014.This work was supported by a contract from the Institució Catalana de Recerca i Estudis Avançats, a European Research Council Starting Grant (ERC-2007-StG-206883), a grant (BFU2011-23434) from Ministerio de Economía y Competitividad (MINECO) to I.R.-T, and a pregraduate Formación del Personal Investigador and a pregraduate Formación Profesorado Universitario grant from MINECO to A.d.M. and A.S.-P.Peer Reviewe

New genomes, new taxa and deep questions in the eukaryotic tree of life: a meeting report on the EMBO comparative genomics conference

A report on the meeting Comparative Genomics of Eukaryotic Microorganisms: understanding the complexity of diversity. Sant Feliu de Guíxols, Spain. October 15-20, 2011

Male Hamsters Discriminate Estrous State From Vaginal Secretions and Individuals From Flank Marks

It is clear that male hamsters discriminate between the odors of individual, conspecific females, as shown by using habituation–dishabituation methods. However, it is not clear from past research whether male hamsters are able to discriminate between the odors of estrous and non-estrous females. A series of habituation–dishabituation experiments was conducted to determine whether males discriminated between different estrous cycle states using two female secretions, those from flank-glands and vaginal secretions. We found that, when habituated to a female flank-gland secretion, males discriminated between this female and a second female on the test trial, whether both were in estrus, both were in diestrus, or one was in estrus and the other in diestrus. There was no difference, however, in the magnitude of their dishabituation response toward flank-gland odors of females in estrus and diestrus. These results suggest that males use flank-gland odors to gain information primarily about individuals. When tested with vaginal secretions in habituation–dishabituation tests, males only showed differences in investigation when the second female was in estrus, indicating that males use vaginal secretions to gain information primarily about reproductive state

GENOME_Capsaspora_annotations.fasta

Annotation of some C. owczarzaki gene

Evolution of the MAGUK protein gene family in premetazoan lineages

Background: Cell-to-cell communication is a key process in multicellular organisms. In multicellular animals, scaffolding proteins belonging to the family of membrane-associated guanylate kinases (MAGUK) are involved in the regulation and formation of cell junctions. These MAGUK proteins were believed to be exclusive to Metazoa. However, a MAGUK gene was recently identified in an EST survey of Capsaspora owczarzaki, an unicellular organism that branches off near the metazoan clade. To further investigate the evolutionary history of MAGUK, we have undertook a broader search for this gene family using available genomic sequences of different opisthokont taxa. Results: Our survey and phylogenetic analyses show that MAGUK proteins are present not only in Metazoa, but also in the choanoflagellate Monosiga brevicollis and in the protist Capsaspora owczarzaki. However, MAGUKs are absent from fungi, amoebozoans or any other eukaryote. The repertoire of MAGUKs in Placozoa and eumetazoan taxa (Cnidaria + Bilateria) is quite similar, except for one class that is missing in Trichoplax, while Porifera have a simpler MAGUK repertoire. However, Vertebrata have undergone several independent duplications and exhibit two exclusive MAGUK classes. Three different MAGUK types are found in both M. brevicollis and C. owczarzaki: DLG, MPP and MAGI. Furthermore, M. brevicollis has suffered a lineage-specific diversification. Conclusions: The diversification of the MAGUK protein gene family occurred, most probably, prior to the divergence between Metazoa+choanoflagellates and the Capsaspora+Ministeria clade. A MAGI-like, a DLG-like, and a MPP-like ancestral genes were already present in the unicellular ancestor of Metazoa, and new gene members have been incorporated through metazoan evolution within two major periods, one before the spongeeumetazoan split and another within the vertebrate lineage. Moreover, choanoflagellates have suffered an independent MAGUK diversification. This study highlights the importance of generating enough genome data from the broadest possible taxonomic sampling, in order to fully understand the evolutionary history of major protein gene families