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Diversity, evolution, and function of myriapod hemocyanins

BACKGROUND: Hemocyanin transports O(2) in the hemolymph of many arthropod species. Such respiratory proteins have long been considered unnecessary in Myriapoda. As a result, the presence of hemocyanin in Myriapoda has long been overlooked. We analyzed transcriptome and genome sequences from all majo...

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Autores principales: Scherbaum, Samantha, Hellmann, Nadja, Fernández, Rosa, Pick, Christian, Burmester, Thorsten
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6034248/
https://www.ncbi.nlm.nih.gov/pubmed/29976142
http://dx.doi.org/10.1186/s12862-018-1221-2
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author Scherbaum, Samantha
Hellmann, Nadja
Fernández, Rosa
Pick, Christian
Burmester, Thorsten
author_facet Scherbaum, Samantha
Hellmann, Nadja
Fernández, Rosa
Pick, Christian
Burmester, Thorsten
author_sort Scherbaum, Samantha
collection PubMed
description BACKGROUND: Hemocyanin transports O(2) in the hemolymph of many arthropod species. Such respiratory proteins have long been considered unnecessary in Myriapoda. As a result, the presence of hemocyanin in Myriapoda has long been overlooked. We analyzed transcriptome and genome sequences from all major myriapod taxa – Chilopoda, Diplopoda, Symphyla, and Pauropoda – with the aim of identifying hemocyanin-like proteins. RESULTS: We investigated the genomes and transcriptomes of 56 myriapod species and identified 46 novel full-length hemocyanin subunit sequences in 20 species of Chilopoda, Diplopoda, and Symphyla, but not Pauropoda. We found in Cleidogona sp. (Diplopoda, Chordeumatida) a hemocyanin-like sequence with mutated copper-binding centers, which cannot bind O(2). An RNA-seq approach showed markedly different hemocyanin mRNA levels from ~ 6 to 25,000 reads per kilobase per million reads. To evaluate the contribution of hemocyanin to O(2) transport, we specifically studied the hemocyanin of the centipede Scolopendra dehaani. This species harbors two distinct hemocyanin subunits with low expression levels. We showed cooperative O(2) binding in the S. dehaani hemolymph, indicating that hemocyanin supports O(2) transport even at low concentration. Further, we demonstrated that hemocyanin is > 1500-fold more highly expressed in the fertilized egg than in the adult. CONCLUSION: Hemocyanin was most likely the respiratory protein in the myriapod stem-lineage, but multiple taxa may have independently lost hemocyanin and thus the ability of efficient O(2) transport. In myriapods, hemocyanin is much more widespread than initially appreciated. Some myriapods express hemocyanin only at low levels, which are, nevertheless, sufficient for O(2) supply. Notably, also in myriapods, a non-respiratory protein similar to insect storage hexamerins evolved from the hemocyanin. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-018-1221-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-60342482018-07-12 Diversity, evolution, and function of myriapod hemocyanins Scherbaum, Samantha Hellmann, Nadja Fernández, Rosa Pick, Christian Burmester, Thorsten BMC Evol Biol Research Article BACKGROUND: Hemocyanin transports O(2) in the hemolymph of many arthropod species. Such respiratory proteins have long been considered unnecessary in Myriapoda. As a result, the presence of hemocyanin in Myriapoda has long been overlooked. We analyzed transcriptome and genome sequences from all major myriapod taxa – Chilopoda, Diplopoda, Symphyla, and Pauropoda – with the aim of identifying hemocyanin-like proteins. RESULTS: We investigated the genomes and transcriptomes of 56 myriapod species and identified 46 novel full-length hemocyanin subunit sequences in 20 species of Chilopoda, Diplopoda, and Symphyla, but not Pauropoda. We found in Cleidogona sp. (Diplopoda, Chordeumatida) a hemocyanin-like sequence with mutated copper-binding centers, which cannot bind O(2). An RNA-seq approach showed markedly different hemocyanin mRNA levels from ~ 6 to 25,000 reads per kilobase per million reads. To evaluate the contribution of hemocyanin to O(2) transport, we specifically studied the hemocyanin of the centipede Scolopendra dehaani. This species harbors two distinct hemocyanin subunits with low expression levels. We showed cooperative O(2) binding in the S. dehaani hemolymph, indicating that hemocyanin supports O(2) transport even at low concentration. Further, we demonstrated that hemocyanin is > 1500-fold more highly expressed in the fertilized egg than in the adult. CONCLUSION: Hemocyanin was most likely the respiratory protein in the myriapod stem-lineage, but multiple taxa may have independently lost hemocyanin and thus the ability of efficient O(2) transport. In myriapods, hemocyanin is much more widespread than initially appreciated. Some myriapods express hemocyanin only at low levels, which are, nevertheless, sufficient for O(2) supply. Notably, also in myriapods, a non-respiratory protein similar to insect storage hexamerins evolved from the hemocyanin. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-018-1221-2) contains supplementary material, which is available to authorized users. BioMed Central 2018-07-05 /pmc/articles/PMC6034248/ /pubmed/29976142 http://dx.doi.org/10.1186/s12862-018-1221-2 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Scherbaum, Samantha
Hellmann, Nadja
Fernández, Rosa
Pick, Christian
Burmester, Thorsten
Diversity, evolution, and function of myriapod hemocyanins
title Diversity, evolution, and function of myriapod hemocyanins
title_full Diversity, evolution, and function of myriapod hemocyanins
title_fullStr Diversity, evolution, and function of myriapod hemocyanins
title_full_unstemmed Diversity, evolution, and function of myriapod hemocyanins
title_short Diversity, evolution, and function of myriapod hemocyanins
title_sort diversity, evolution, and function of myriapod hemocyanins
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6034248/
https://www.ncbi.nlm.nih.gov/pubmed/29976142
http://dx.doi.org/10.1186/s12862-018-1221-2
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