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The Queen Conch (Lobatus gigas) Proteome: A Valuable Tool for Biological Studies in Marine Gastropods

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Abstract

Queen conch (Lobatus gigas) is a marine gastropod endemic to the Caribbean. This species is a cultural symbol, being a significant local food source and the second largest commercial fishery in the region. However, over-exploitation and natural habitat degradation have exerted high survival pressure on this species. This work aims to provide novel proteomic data to highlight the metabolism of the species and to provide an important tool for the understanding of queen conch biology and physiology. Herein, we profiled the whole proteome from 3 organs (gills, digestive gland and muscle) of L. gigas combining gel-free and gel-based techniques. Overall 420 clusters of proteins were identified corresponding to the minimum identification requirement of protein sequence redundancy. Gene ontology and KEGG analysis highlighted 59 metabolic pathways between identified proteins. The most relevant routes according to the number of sequences found per pathway were purine and thiamine metabolism, closely related to nucleotide and carbohydrate metabolism. We also emphasize the high number of proteins associated to the biosynthesis of antibiotics (93 proteins and a total of 28 enzymes), which were among the top-twenty pathways identified by KEGG analysis. The proteomics approach allowed the identification and description of putative markers of oxidative stress, xenobiotic metabolism, heat shock response and respiratory chain for the first time in the species, which could be extremely useful in future investigations for diagnosing and monitoring L. gigas population health.

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Fig. 1

Photo Courtesy of Joan Hernandez Albernas taken at the Buenavista Biosphere Reserve, Cayo Santa Maria Wildlife Refuge, Villa Clara, Cuba

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References

  1. Ríos-Jara E, Pérez-Peña M, Beas-Luna R, López-Uriarte E, Juárez-Carrillo E (2001) Gastropods and bivalves of commercial interest from the continental shelf of Jalisco and Colima, México. Rev Biol Trop 49:859–863

    PubMed  Google Scholar 

  2. Wilson S, Street S, Sato T (2005) Discarded queen conch (Strombus gigas) shells as shelter sites for fish. Mar Biol 147:179–188

    Article  Google Scholar 

  3. Sterrer W (1986) Marine fauna and flora of Bermuda: a systematic guide to the identification of marine organisms. Wiley-Interscience, New York

    Google Scholar 

  4. Whitall D et al (2016) Contaminants in queen conch (Strombus gigas) in Vieques, Puerto Rico. Reg Stud Mar Sci 5:80–86

    Article  Google Scholar 

  5. Volland JM, Gros O (2012) Cytochemical investigation of the digestive gland of two strombidae species (Strombus gigas and Strombus pugilis) in relation to the nutrition. Microsc Res Tech 75:1353–1360

    Article  CAS  PubMed  Google Scholar 

  6. Cuartas JH, Alzate JF, Moreno-Herrera CX, Marquez EJ (2018) Metagenomic analysis of orange colored protrusions from the muscle of Queen Conch Lobatus gigas (Linnaeus, 1758). PeerJ 6:e4307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Stoner A, Davis M, Booker C (2012) Evidence for a significant decline in queen conch in the Bahamas, including the population in a marine protected area. Proc Gulf Carib Fish Inst 64:349–361

    Google Scholar 

  8. Stoner A, Ray M (1996) Queen conch, Strombus gigas, in fished and unfished locations of the Bahamas: effects of a marine fishery reserve on adults, juveniles, and larval production. Fishery Bull 94:551–556

    Google Scholar 

  9. Brownell WN, Stevely JM (1981) The biology, fisheries, and management of the queen conch, Strombus gigas. Mar Fisheries Rev 43:1–12

    Google Scholar 

  10. Hernandez-Lamb J, Dibello A, Lewis S, Mackin G, Kirby K, Acosta C (2012) Modelling the effects of reserve size and fishing mortality for Caribbean queen conch Strombus gigas. Aquat Conserv 22:721–730

    Article  Google Scholar 

  11. Glazer RA, Quintero I (1998) Observations on the sensitivity of queen conch to water quality: implications for coastal development. Proc Gulf Caribb Fish Inst 50:78–93

    Google Scholar 

  12. Delgado GA, Bartels CT, Glazer RA, Brown-Peterson NJ, McCarthy KJ (2004) Translocation as a strategy to rehabilitate the queen conch (Strombus gigas) population in the Florida Keys. Fish Bull 102:278–288

    Google Scholar 

  13. McCarthy KJ, Bartels CT, Darcy MC, Delgado GA, Glazer RA (2002) Preliminary observation of reproductive failure in nearshore queen conch (Strombus gigas) in the Florida Keys. Proc Gulf Carib Fish Inst 53:674–680

    Google Scholar 

  14. NOAA (2012) Queen conch, Strombus gigas (Linnaeus 1758) status report. National Oceanic and Atmospheric Administration (NOAA), Washington

  15. Peel JR, Mandujano MdC (2014) Impact of minimum catch size on the population viability of Strombus gigas (Mesogastropoda: Strombidae) in Quintana Roo, Mexico. Rev Biol Trop 62:1343–1352

    Article  PubMed  Google Scholar 

  16. Aranda DA et al (2014) Reproductive patterns of queen conch, Strombus gigas (Mollusca, Gastropoda), across the wider Caribbean Region. Bull Mar Sci 90:813–831

    Article  Google Scholar 

  17. Cárdenas EA, Aranda DA (2014) Growth parameters and density variation of a queen conch, Strombus gigas (Neotaenioglossa: Strombidae), population from Xel-Há park, a marine protected area. Rev Biol Trop 62:59–72

    Google Scholar 

  18. Aranda DA, Chávez Villegas JF, Sánchez Crespo M (2014) Is the Queen conch Strombus gigas (Mesogastropoda: Strombidae) a species with Allee effect? Rev Biol Trop 62:373–378

    Google Scholar 

  19. Stoner AW, Ray-Culp M (2000) Evidence for Allee effects in an over-harvested marine gastropod: density-dependent mating and egg production. Mar Ecol Prog Ser 202:297–302

    Article  Google Scholar 

  20. Marquez EJ, Restrepo-Escobar N, Montoya-Herrera FL (2016) Shell shape variation of queen conch Strombus gigas (Mesograstropoda: Strombidae) from Southwest Caribbean. Rev Biol Trop 64:1585–1595

    Article  PubMed  Google Scholar 

  21. Pérez-Enriquez R, Garcia-Rodriguez FJ, Mendoza-Carrion G, Padilla C (2011) Geographical variation in the genetic diversity and composition of the endangered queen conch Strombus gigas (Mesogastropoda: Strombidae) from Yucatán, México. Rev Biol Trop 59:1115–1126

    PubMed  Google Scholar 

  22. Garr AL, Acosta-Salmón H, Riche M, Davis M, Capo TR, Haley D, Tracy P (2011) Growth and survival of juvenile queen conch Strombus gigas fed artificial diets containing varying levels of digestible protein and energy. North Am J Aquac 73:34–41

    Google Scholar 

  23. Sale P et al (2010) Conservando la conectividad de los arrecifes: guía para los administradores de las áreas marinas protegidas. UNU-INWEH, Canada

    Google Scholar 

  24. Aranda DA, Manzano NB (2017) Effects of near-future-predicted ocean temperatures on early development and calcification of the queen conch Strombus gigas. Aquac Int 25:1869–1881

    Article  Google Scholar 

  25. Titley-O’Neal CP, Spade DJ, Zhang Y, Kan R, Martyniuk CJ, Denslow ND, MacDonald BA (2013) Gene expression profiling in the ovary of queen conch (Strombus gigas) exposed to environments with high tributyltin in the British Virgin Islands. Sci Total Environ 449:52–62

    Article  PubMed  CAS  Google Scholar 

  26. Delgado GA, Glazer RA, Wetzel D (2013) Effects of mosquito control pesticides on competent queen conch (Strombus gigas) larvae. Biol Bull 225:79–84

    Article  PubMed  Google Scholar 

  27. Rizo OD et al (2010) Copper, Zinc and Lead Bioaccumulation in Marine Snail, Strombus gigas, from Guacanayabo Gulf, Cuba. Bull Environ Contam Toxicol 85:330–333

    Article  CAS  Google Scholar 

  28. Spade DJ et al (2010) Queen conch (Strombus gigas) testis regresses during the reproductive season at nearshore sites in the Florida Keys. PLoS ONE 5:e12737

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Campos AM, de Almeida AM (2016) Top-down proteomics and farm animal and aquatic sciences. Proteomes 4:38

    Article  PubMed Central  CAS  Google Scholar 

  30. Heyliger H (1995) Fisheries Regulations 1995 In: Saint Christopher and Nevis Statu-tory Rules and Orders. vol 11

  31. Tiley K, Freeman MA, Dennis MM (2018) Pathology and reproductive health of queen conch (Lobatus gigas) in St. Kitts. J Invertebr Pathol 155:32–37

    Article  PubMed  Google Scholar 

  32. Campos A, Puerto M, Prieto A, Cameán A, Almeida AM, Coelho AV, Vasconcelos V (2013) Protein extraction and two‐dimensional gel electrophoresis of proteins in the marine mussel Mytilus galloprovincialis: an important tool for protein expression studies, food quality and safety assessment J Sci Food Agric 93:1779–1787

    Article  PubMed  CAS  Google Scholar 

  33. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680

    Article  CAS  PubMed  Google Scholar 

  34. Bergfelt DR et al (2018) Preliminary analysis of the proteome of exhaled breath condensate in Bottlenose Dolphins (Tursiops truncatus). Aquat Mamm 44:256–266

    Article  Google Scholar 

  35. Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359

    Article  PubMed  CAS  Google Scholar 

  36. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, Olsen JV, Mann M (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc 4:698

    Article  CAS  PubMed  Google Scholar 

  37. Jungo F, Estreicher A, Bairoch A, Bougueleret L, Xenarios I (2010) Animal toxins: how is complexity represented in databases? Toxins 2:262–282

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  39. Kanehisa M et al (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:D354–357

    Article  CAS  PubMed  Google Scholar 

  40. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–185

    Article  PubMed  PubMed Central  Google Scholar 

  41. Tyanova S, Temu T, Cox J (2016) The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc 11:2301

    Article  CAS  PubMed  Google Scholar 

  42. Domínguez-Pérez D et al (2018) Proteomic analyses of the unexplored sea anemone Bunodactis verrucosa. Mar Drugs 16:42

    Article  PubMed Central  CAS  Google Scholar 

  43. Frazão B et al (2017) Analysis of Pelagia noctiluca proteome reveals a red fluorescent protein, a zinc metalloproteinase and a peroxiredoxin. Protein J 36:77–97

    Article  PubMed  CAS  Google Scholar 

  44. Gochfeld DJ, Ankisetty S, Slattery M (2015) Proteomic profiling of healthy and diseased hybrid soft corals Sinularia maxima × S. polydactyla. Dis Aquat Org 116:133–141

    Article  Google Scholar 

  45. Cha IS, del Castillo CS, Nho SW, Hikima J-i, Aoki T, Jung TS (2011) Innate immune response in the hemolymph of an ascidian, Halocynthia roretzi, showing soft tunic syndrome, using label-free quantitative proteomics. Dev Comp Immunol 35:809–816

    Article  CAS  PubMed  Google Scholar 

  46. Zhang D-M et al (2016) Nano-LC-ESI MS/MS analysis of proteins in dried sea dragon Solenognathus hardwickii and bioinformatic analysis of its protein expression profiling. Chin J Mater Med 14:709–713

    CAS  Google Scholar 

  47. Miller BA et al. (2017) Plasma proteome and clinical biochemistry associated with performance-based physical activity in bottlenose dolphins (Tursiops truncatus) Aquat Mamm 43:453

    Article  Google Scholar 

  48. Márquez EJ, Castro ER, Alzate JF (2016) Mitochondrial genome of the endangered marine gastropod Strombus gigas Linnaeus, 1758 (Mollusca: Gastropoda). Mitochondr DNA 27:1516–1517

    Article  CAS  Google Scholar 

  49. Boggs I, Hine B, Smolenski G, Hettinga K, Zhang L, Wheeler TT (2016) Proteomics data in support of the quantification of the changes of bovine milk proteins during mammary gland involution. Data Brief 8:52–55

    Article  PubMed  PubMed Central  Google Scholar 

  50. Eastlake K et al (2017) Comparison of proteomic profiles in the zebrafish retina during experimental degeneration and regeneration. Sci Rep 7:44601

    Article  PubMed  PubMed Central  Google Scholar 

  51. Wang H, Chang-Wong T, Tang H-Y, Speicher DW (2010) Comparison of extensive protein fractionation and repetitive LC-MS/MS analyses on depth of analysis for complex proteomes. J Proteome Res 9:1032–1040

    Article  CAS  PubMed  Google Scholar 

  52. Lonsdale D (2006) A review of the biochemistry, metabolism and clinical benefits of thiamin (e) and its derivatives. Evid Based Complement Alternat Med 3:49–59

    Article  PubMed  PubMed Central  Google Scholar 

  53. Moffatt BA, Ashihara H (2002) Purine and pyrimidine nucleotide synthesis and metabolism. Arabidopsis Book 1:e0018

    Article  PubMed  PubMed Central  Google Scholar 

  54. Banaszak AT, García Ramos M, Goulet TL (2013) The symbiosis between the gastropod Strombus gigas and the dinoflagellate Symbiodinium: an ontogenic journey from mutualism to parasitism. J Exp Mar Biol Ecol 449:358–365

    Article  Google Scholar 

  55. Ramos MG, Banaszak AT (2014) Symbiotic association between Symbiodinium and the gastropod Strombus gigas: larval acquisition of symbionts. Mar Biotechnol 16:193–201

    Article  CAS  Google Scholar 

  56. Acosta EA, Gómez E, Romero Tabarez M, Cadavid Restrepo GE, Moreno Herrera CX (2009) Identificación molecular de poblaciones bacterianas asociadas al caracol pala (Strombus gigas) del caribe colombiano. Acta Biol Colomb 14:83–96

    Google Scholar 

  57. Carrascal OMP, Elorza MP, Restrepo GEC, Herrera CXM (2014) Assessment of the bacterial community diversity associated with the queen conch Strombus gigas (Linnaeus, 1758) from the Caribbean coast of Colombia using denaturing gradient gel electrophoresis and culturing. Aquac Res 45:773–786

    Article  CAS  Google Scholar 

  58. Rodriguez AI, Hariharan H, Nimrod S (2011) Occurrence and antimicrobial drug resistance of potential bacterial pathogens from shellfish, including queen conchs (Strombus gigas) and whelks (Cittarium pica) in Grenada. Webmed Cent Microbiol 2:WMC001943

  59. Azevedo CC, Guzman-Guillen R, Martins JC, Osorio H, Vasconcelos V, da Fonseca RR, Campos A (2015) Proteomic profiling of gill GSTs in Mytilus galloprovincialis from the North of Portugal and Galicia evidences variations at protein isoform level with a possible relation with water quality. Mar Environ Res 110:152–161

    Article  CAS  PubMed  Google Scholar 

  60. Carneiro M, Reis B, Azevedo J, Campos A, Osorio H, Vasconcelos V, Martins JC (2015) Glutathione transferases responses induced by microcystin-LR in the gills and hepatopancreas of the clam Venerupis philippinarum. Toxins (Basel) 7:2096–2120

    Article  CAS  Google Scholar 

  61. Tomanek L, Zuzow MJ, Hitt L, Serafini L, Valenzuela JJ (2012) Proteomics of hyposaline stress in blue mussel congeners (genus Mytilus): implications for biogeographic range limits in response to climate change. J Exp Biol 215:3905–3916

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was developed under the post-doctoral grant to A Campos (SFRH_BPD_103683_2014) funded by Portuguese Science Foundation (Fundação para a Ciência e a Tecnologia, FCT) and under the Projects MOREBIVALVES (PTDC/ASP-PES/31762/2017) and UID/Multi/04423/2013 co-financed by NORTE 2020, Portugal 2020 and the European Union through the ERDF, and by FCT. Authors thank Ross University School of Veterinary Medicine (Basseterre, St. Kitts and Nevis) for the logistics support that allowed the conduction of this research.

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Authors and Affiliations

  1. CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450–238, Matosinhos, Portugal

    Dany Domínguez-Pérez, Vitor Vasconcelos & Alexandre Campos

  2. United States Department of Agriculture, Ames, IA, USA

    John Lippolis

  3. Ross University School of Veterinary Medicine, Baseterre, St. Kitts and Nevis

    Michelle Dennis, Blake Miller & Katie Tiley

  4. Department of Biology, Faculty of Sciences, University of Porto, Porto, Portugal

    Vitor Vasconcelos

  5. Instituto Superior de Agronomia, Universidade de Lisboa, Lisbon, Portugal

    André M. de Almeida

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  1. Dany Domínguez-Pérez
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  3. Michelle Dennis
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Correspondence to Alexandre Campos.

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All authors have disclosed any actual or potential competing interests (financial or non-financial) regarding the content of this article.

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All experiments were conducted in accordance with ethical guidelines of the European Union Council (Directives 86/609/EEC and 2010/63/EU) and the Portuguese Agricultural Ministry (Portaria nr.1005/92 of 23 October 2010) for the protection of animals used for experimental and other scientific purposes.

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Domínguez-Pérez, D., Lippolis, J., Dennis, M. et al. The Queen Conch (Lobatus gigas) Proteome: A Valuable Tool for Biological Studies in Marine Gastropods. Protein J 38, 628–639 (2019). https://doi.org/10.1007/s10930-019-09857-0

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