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High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders

BACKGROUND: Spiders are known for their predatory efficiency and for their high capacity of digesting relatively large prey. They do this by combining both extracorporeal and intracellular digestion. Whereas many high throughput (“-omics”) techniques focus on biomolecules in spider venom, so far thi...

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Autores principales: Fuzita, Felipe J., Pinkse, Martijn W. H., Patane, José S. L., Verhaert, Peter D. E. M., Lopes, Adriana R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5013568/
https://www.ncbi.nlm.nih.gov/pubmed/27604083
http://dx.doi.org/10.1186/s12864-016-3048-9
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author Fuzita, Felipe J.
Pinkse, Martijn W. H.
Patane, José S. L.
Verhaert, Peter D. E. M.
Lopes, Adriana R.
author_facet Fuzita, Felipe J.
Pinkse, Martijn W. H.
Patane, José S. L.
Verhaert, Peter D. E. M.
Lopes, Adriana R.
author_sort Fuzita, Felipe J.
collection PubMed
description BACKGROUND: Spiders are known for their predatory efficiency and for their high capacity of digesting relatively large prey. They do this by combining both extracorporeal and intracellular digestion. Whereas many high throughput (“-omics”) techniques focus on biomolecules in spider venom, so far this approach has not yet been applied to investigate the protein composition of spider midgut diverticula (MD) and digestive fluid (DF). RESULTS: We here report on our investigations of both MD and DF of the spider Nephilingis (Nephilengys) cruentata through the use of next generation sequencing and shotgun proteomics. This shows that the DF is composed of a variety of hydrolases including peptidases, carbohydrases, lipases and nuclease, as well as of toxins and regulatory proteins. We detect 25 astacins in the DF. Phylogenetic analysis of the corresponding transcript(s) in Arachnida suggests that astacins have acquired an unprecedented role for extracorporeal digestion in Araneae, with different orthologs used by each family. The results of a comparative study of spiders in distinct physiological conditions allow us to propose some digestion mechanisms in this interesting animal taxon. CONCLUSION: All the high throughput data allowed the demonstration that DF is a secretion originating from the MD. We identified enzymes involved in the extracellular and intracellular phases of digestion. Besides that, data analyses show a large gene duplication event in Araneae digestive process evolution, mainly of astacin genes. We were also able to identify proteins expressed and translated in the digestive system, which until now had been exclusively associated to venom glands. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3048-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-50135682016-09-08 High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders Fuzita, Felipe J. Pinkse, Martijn W. H. Patane, José S. L. Verhaert, Peter D. E. M. Lopes, Adriana R. BMC Genomics Research Article BACKGROUND: Spiders are known for their predatory efficiency and for their high capacity of digesting relatively large prey. They do this by combining both extracorporeal and intracellular digestion. Whereas many high throughput (“-omics”) techniques focus on biomolecules in spider venom, so far this approach has not yet been applied to investigate the protein composition of spider midgut diverticula (MD) and digestive fluid (DF). RESULTS: We here report on our investigations of both MD and DF of the spider Nephilingis (Nephilengys) cruentata through the use of next generation sequencing and shotgun proteomics. This shows that the DF is composed of a variety of hydrolases including peptidases, carbohydrases, lipases and nuclease, as well as of toxins and regulatory proteins. We detect 25 astacins in the DF. Phylogenetic analysis of the corresponding transcript(s) in Arachnida suggests that astacins have acquired an unprecedented role for extracorporeal digestion in Araneae, with different orthologs used by each family. The results of a comparative study of spiders in distinct physiological conditions allow us to propose some digestion mechanisms in this interesting animal taxon. CONCLUSION: All the high throughput data allowed the demonstration that DF is a secretion originating from the MD. We identified enzymes involved in the extracellular and intracellular phases of digestion. Besides that, data analyses show a large gene duplication event in Araneae digestive process evolution, mainly of astacin genes. We were also able to identify proteins expressed and translated in the digestive system, which until now had been exclusively associated to venom glands. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3048-9) contains supplementary material, which is available to authorized users. BioMed Central 2016-09-07 /pmc/articles/PMC5013568/ /pubmed/27604083 http://dx.doi.org/10.1186/s12864-016-3048-9 Text en © The Author(s). 2016 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
Fuzita, Felipe J.
Pinkse, Martijn W. H.
Patane, José S. L.
Verhaert, Peter D. E. M.
Lopes, Adriana R.
High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders
title High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders
title_full High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders
title_fullStr High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders
title_full_unstemmed High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders
title_short High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders
title_sort high throughput techniques to reveal the molecular physiology and evolution of digestion in spiders
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5013568/
https://www.ncbi.nlm.nih.gov/pubmed/27604083
http://dx.doi.org/10.1186/s12864-016-3048-9
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