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PLoS One
2015 Jan 01;108:e0129668. doi: 10.1371/journal.pone.0129668.
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Phylogeny of Echinoderm Hemoglobins.
Christensen AB
,
Herman JL
,
Elphick MR
,
Kober KM
,
Janies D
,
Linchangco G
,
Semmens DC
,
Bailly X
,
Vinogradov SN
,
Hoogewijs D
.
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BACKGROUND: Recent genomic information has revealed that neuroglobin and cytoglobin are the two principal lineages of vertebrate hemoglobins, with the latter encompassing the familiar myoglobin and α-globin/β-globin tetramer hemoglobin, and several minor groups. In contrast, very little is known about hemoglobins in echinoderms, a phylum of exclusively marine organisms closely related to vertebrates, beyond the presence of coelomic hemoglobins in sea cucumbers and brittle stars. We identified about 50 hemoglobins in sea urchin, starfish and sea cucumber genomes and transcriptomes, and used Bayesian inference to carry out a molecular phylogenetic analysis of their relationship to vertebrate sequences, specifically, to assess the hypothesis that the neuroglobin and cytoglobin lineages are also present in echinoderms.
RESULTS: The genome of the sea urchin Strongylocentrotus purpuratus encodes several hemoglobins, including a unique chimeric 14-domain globin, 2 androglobin isoforms and a unique single androglobin domain protein. Other strongylocentrotid genomes appear to have similar repertoires of globin genes. We carried out molecular phylogenetic analyses of 52 hemoglobins identified in sea urchin, brittle star and sea cucumber genomes and transcriptomes, using different multiple sequence alignment methods coupled with Bayesian and maximum likelihood approaches. The results demonstrate that there are two major globin lineages in echinoderms, which are related to the vertebrate neuroglobin and cytoglobin lineages. Furthermore, the brittle star and sea cucumber coelomic hemoglobins appear to have evolved independently from the cytoglobin lineage, similar to the evolution of erythroid oxygen binding globins in cyclostomes and vertebrates.
CONCLUSION: The presence of echinoderm globins related to the vertebrate neuroglobin and cytoglobin lineages suggests that the split between neuroglobins and cytoglobins occurred in the deuterostome ancestor shared by echinoderms and vertebrates.
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26247465
???displayArticle.pmcLink???PMC4527676 ???displayArticle.link???PLoS One
Fig 1. Bayesian phylogenetic tree based on a MAFFT L-INS-i MSA of 52 Echinoderm Hbs.
Fig 2. Bayesian phylogenetic tree based on a MAFFT L-INS-i MSA of 36 Echinoderm Hbs and 30 Vertebrate Hbs, using the Bacillus nonheme globin sequence [56], as outgroup.
Fig 3. Bayesian phylogenetic tree based on a T-Coffee Expresso MSA of 36 Echinoderm Hbs and 30 Vertebrate Hbs, using the Bacillus nonheme globin sequence [56], as outgroup.
Fig 4. Bayesian phylogenetic tree based on a Clustal Omega MSA of 36 Echinoderm Hbs and 30 Vertebrate Hbs, using the Bacillus nonheme globin sequence [56], as outgroup.
Fig 5. (A) Consensus tree generated by StructAlign, which carries out joint Bayesian inference of alignments and trees under a joint model of sequence and structure evolution.The structures used here correspond to echinoderm coelomic Hbs (1hlb,1hlm), vertebrate Ngb (1oj6), Cygb (1urv), Mb (2mm1), HbA (2hhb) C. elegans Ngb (3mvc), plant Hbs (2oif, 1lh1), and two bacterial SDgbs (3s1j,2wy4). (B) Tree generated using a larger dataset, consisting of the aforementioned structures augmented with cyclostome Hbs (2lhb, 1it2) A. limacina Mb (1mba), D. melanogaster Hb (2g3h), G. intestinalis Hb (1c0k), C. elegans Glb-1 (2wtg), C. lacteus Ngb (2xki), and an bacterial non-heme globin (1bnl) as an outgroup.
Fig 6. Structural superposition of the echinoderm structure 1hlm (brown) with the cytoglobin structure 1urv (blue).The two structures show a very close correspondence, with some localized deviations, such as at helix D, which is disordered in 1hlm (marked by Arg65), and at the C-terminal end of helix G (marked by Val131).
Fig 7. Analysis of average per-site root mean square deviation (RMSD) between the echinoderm structures (1hlb, 1hlm) and the Ngb (1oj6) and Cygb (1urv) structures.Structural deviation was computed from each of the echinoderms to the target structure of interest as described in the Methods section, using the consensus alignment generated on the larger structural dataset; the mean of these two values computed for each column. Colored blocks at the bottom indicate charged (red) and non-charged (black) residues. Gaps are shown in grey, and the proximal and distal histidines are shown in blue. Helix locations are annotated above, and named using standard conventions. Overall RMSD for each plot is computed as the mean of the squared contributions from each site, and is indicated by the dashed red line. The blue areas underneath indicate the confidence associated with each column in the multiple alignment, as outputted by StructAlign.
Fig 8. Analysis of pairwise per-site root mean square deviation (RMSD) between the echinoderm structures (1hlb, 1hlm) and the Ngb (1oj6) and Cygb (1urv) structures.Colored blocks at the bottom indicate charged (red) and non-charged (black) residues. Gaps are shown in grey, and the proximal and distal histidines are shown in blue. Helix locations are annotated above, and names using standard conventions. Overall RMSD for each plot is computed as the mean of the squared contributions from each site, and is indicated by the dashed red line. The blue areas underneath indicate the confidence associated with each column in the multiple alignment, as outputted by StructAlign.
Abascal,
ProtTest: selection of best-fit models of protein evolution.
2005, Pubmed
Abascal,
ProtTest: selection of best-fit models of protein evolution.
2005,
Pubmed
Baker,
Hemoglobin Structure and Function in the Rat-Tailed Sea Cucumber, Paracaudina chilensis.
1993,
Pubmed
,
Echinobase
Bashford,
Determinants of a protein fold. Unique features of the globin amino acid sequences.
1987,
Pubmed
Blank,
A membrane-bound vertebrate globin.
2011,
Pubmed
Bonaventura,
Functional consequences of ligand-linked dissociation in hemoglobin from the sea cucumber Molpadia arenicola.
1976,
Pubmed
,
Echinobase
Bottjer,
Paleogenomics of echinoderms.
2006,
Pubmed
,
Echinobase
Burmester,
Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues.
2002,
Pubmed
Burmester,
A vertebrate globin expressed in the brain.
2000,
Pubmed
Burmester,
What is the function of neuroglobin?
2009,
Pubmed
Cameron,
SpBase: the sea urchin genome database and web site.
2009,
Pubmed
,
Echinobase
Challis,
A stochastic evolutionary model for protein structure alignment and phylogeny.
2012,
Pubmed
Christensen,
Functional and biochemical properties of the hemoglobins of the burrowing brittle star Hemipholis elongata say (Echinodermata, Ophiuroidea).
2003,
Pubmed
,
Echinobase
Di Tommaso,
T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension.
2011,
Pubmed
Do,
ProbCons: Probabilistic consistency-based multiple sequence alignment.
2005,
Pubmed
Dröge,
Phylogenetic analysis reveals wide distribution of globin X.
2011,
Pubmed
Du,
Transcriptome sequencing and characterization for the sea cucumber Apostichopus japonicus (Selenka, 1867).
2012,
Pubmed
,
Echinobase
Edgar,
MUSCLE: multiple sequence alignment with high accuracy and high throughput.
2004,
Pubmed
Fuchs,
The amphibian globin gene repertoire as revealed by the Xenopus genome.
2006,
Pubmed
Hankeln,
Neuroglobin and cytoglobin in search of their role in the vertebrate globin family.
2005,
Pubmed
Herman,
Simultaneous Bayesian estimation of alignment and phylogeny under a joint model of protein sequence and structure.
2014,
Pubmed
Hoffmann,
Differential loss and retention of cytoglobin, myoglobin, and globin-E during the radiation of vertebrates.
2011,
Pubmed
Hoffmann,
Evolution of the globin gene family in deuterostomes: lineage-specific patterns of diversification and attrition.
2012,
Pubmed
,
Echinobase
Hoffmann,
Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates.
2010,
Pubmed
Hoogewijs,
A phylogenetic analysis of the globins in fungi.
2012,
Pubmed
Hoogewijs,
Androglobin: a chimeric globin in metazoans that is preferentially expressed in Mammalian testes.
2012,
Pubmed
Katoh,
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.
2013,
Pubmed
Kawada,
Characterization of a stellate cell activation-associated protein (STAP) with peroxidase activity found in rat hepatic stellate cells.
2001,
Pubmed
Kitto,
Evolution of cooperativity in hemoglobins: what can invertebrate hemoglobins tell us?
1998,
Pubmed
,
Echinobase
Kober,
Phylogenomics of strongylocentrotid sea urchins.
2013,
Pubmed
,
Echinobase
Kondo,
Current Status of Echinoderm Genome Analysis - What do we Know?
2012,
Pubmed
,
Echinobase
Kugelstadt,
Neuroglobin, cytoglobin, and a novel, eye-specific globin from chicken.
2004,
Pubmed
Lechauve,
Neuroglobins, pivotal proteins associated with emerging neural systems and precursors of metazoan globin diversity.
2013,
Pubmed
Manwell,
Sea cucumber sibling species: polypeptide chain types and oxygen equilibrium of hemoglobin.
1966,
Pubmed
,
Echinobase
MANWELL,
Oxygen equilibrium of Cucumaria miniata hemoglobin and the absence of the Bohr effect.
1959,
Pubmed
,
Echinobase
MANWELL,
Comparative physiology: blood pigments.
1960,
Pubmed
Mauri,
Amino acid sequence of a globin from the sea cucumber Caudina (Molpadia) arenicola.
1991,
Pubmed
,
Echinobase
McDonald,
Amino acid sequence of the coelomic C globin from the sea cucumber Caudina (Molpadia) arenicola.
1992,
Pubmed
,
Echinobase
Mitchell,
Structural analysis of monomeric hemichrome and dimeric cyanomet hemoglobins from Caudina arenicola.
1995,
Pubmed
,
Echinobase
Murray,
Structure of a nonheme globin in environmental stress signaling.
2005,
Pubmed
Parkhurst,
Kinetics of carbon monoxide binding to the cooperative dimeric hemoglobin from Thyonella gemmata. Analysis of carbon monoxide equilibrium results.
1979,
Pubmed
,
Echinobase
Penn,
An alignment confidence score capturing robustness to guide tree uncertainty.
2010,
Pubmed
Penn,
GUIDANCE: a web server for assessing alignment confidence scores.
2010,
Pubmed
Roesner,
A globin gene of ancient evolutionary origin in lower vertebrates: evidence for two distinct globin families in animals.
2005,
Pubmed
Ronquist,
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.
2012,
Pubmed
Rowe,
The neuropeptide transcriptome of a model echinoderm, the sea urchin Strongylocentrotus purpuratus.
2012,
Pubmed
,
Echinobase
Schäffer,
Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements.
2001,
Pubmed
Shi,
FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties.
2001,
Pubmed
Sievers,
Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega.
2011,
Pubmed
Smith,
Hemoglobins in the genome of the cryptomonad Guillardia theta.
2014,
Pubmed
Sodergren,
The genome of the sea urchin Strongylocentrotus purpuratus.
2006,
Pubmed
,
Echinobase
Stamatakis,
A rapid bootstrap algorithm for the RAxML Web servers.
2008,
Pubmed
Steinmeier,
Oxygen and carbon monoxide equilibria and the kinetics of oxygen binding by the cooperative dimeric hemoglobin of Thyonella gemmata.
1979,
Pubmed
,
Echinobase
Storz,
Phylogenetic diversification of the globin gene superfamily in chordates.
2011,
Pubmed
Storz,
Gene duplication, genome duplication, and the functional diversification of vertebrate globins.
2013,
Pubmed
Suzuki,
Amino acid sequence of a major globin from the sea cucumber Paracaudina chilensis.
1989,
Pubmed
,
Echinobase
Tamura,
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
2011,
Pubmed
Terwilliger,
The hemoglobin of the holothurian echinoderm, Molpadia oölitica Pourtales.
1972,
Pubmed
,
Echinobase
Terwilliger,
Oxygen equilibrium and subunit aggregation of a holothurian hemoglobin.
1975,
Pubmed
,
Echinobase
Trent,
A ubiquitously expressed human hexacoordinate hemoglobin.
2002,
Pubmed
Tu,
Gene structure in the sea urchin Strongylocentrotus purpuratus based on transcriptome analysis.
2012,
Pubmed
,
Echinobase
Vinogradov,
Microbial eukaryote globins.
2013,
Pubmed
Vinogradov,
A phylogenomic profile of globins.
2006,
Pubmed
Vinogradov,
Phylogenetic relationships of 3/3 and 2/2 hemoglobins in Archaeplastida genomes to bacterial and other eukaryote hemoglobins.
2011,
Pubmed
Vinogradov,
Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life.
2005,
Pubmed
Vinogradov,
Bacterial and archaeal globins - a revised perspective.
2013,
Pubmed
Weber,
Nonvertebrate hemoglobins: functions and molecular adaptations.
2001,
Pubmed
Whelan,
A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach.
2001,
Pubmed
Wilson,
SUPERFAMILY--sophisticated comparative genomics, data mining, visualization and phylogeny.
2009,
Pubmed