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Growth Performance and Transcriptomic Response of Warm-Acclimated Hybrid Abalone Haliotis rufescens (♀) × H. corrugata (♂)

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Abstract

Along the Pacific coast of the Baja California Peninsula (Mexico), abalone represents one of the most lucrative fisheries. As wild populations are currently depleted, abalone farm production aims to balance the decreasing populations with the increasing demand. The Mexican abalone aquaculture is almost entirely based on red abalone (Haliotis rufescens). However, the increasing frequency of extreme temperature events is hampering this activity. The use interspecific hybrids can potentially improve abalone culture, as species have differences in their thermal tolerance. Therefore, the hybrid progeny between H. rufescens (♀) and pink abalone H. corrugata (♂), a temperate and a warmer water abalone species, respectively, will naturally support higher temperature. To test this hypothesis, growth rate, mortality and metabolic rate of both pure (RR) and hybrid abalone (RP) were assessed under the H. rufescens’ optimum (18 °C) and thermally stressed (22 °C) conditions. To unveil the molecular pathways involved in the heat response, transcriptional profiling of both crosses was also investigated. At high temperature, we observed constrained growth and survival in RR while RP showed a significant increase in both rates, supporting the improved performance of the hybrid compared. These results match with the transcriptional profiling of hybrids showing higher expression of genes involved in growth and calcification, whereas in the pure red progeny, the transcriptional profile was mainly associated with the regulation of necroptosis process. Our results may contribute to propose new management plans to increase farm abalone production in Baja California.

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Data Availability

All data are fully available without restriction as supplementary material. Raw sequencing data is available at NCBI SRA archive from the GenBank database under the accession numbers SRR10858532 to SRR10858543.

References

  • Alexa A, Rahnenführer J (2009) Gene set enrichment analysis with topGO. Bioconductor Improv 27

  • Alter K, Andrewartha SJ, Morash AJ, Clark TD, Hellicar AD, León RI, Elliott NG (2017) Hybrid abalone are more robust to multi-stressor environments than pure parental species. Aquaculture 478:25–34

    Article  Google Scholar 

  • Andrews S (2012) FastQC: a quality control tool for high throughput sequence data. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

  • Belizário J, Vieira-Cordeiro L, Enns S (2015) Necroptotic cell death signaling and execution pathway: lessons from knockout mice. Mediat Inflamm 2015:1–15

    Article  CAS  Google Scholar 

  • Boch CA, Micheli F, AlNajjar M, Monismith S, Beers J, Bonilla JC et al (2018) Local oceanographic variability influences the performance of juvenile abalone under climate change. Sci Rep 1–12:5501

    Article  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482

    Article  CAS  PubMed  Google Scholar 

  • Chen N, Luo X, Gu Y, Han G, Dong Y, You W, Ke C (2016) Assessment of the thermal tolerance of abalone based on cardiac performance in Haliotis discus hannai, H. gigantea and their interspecific hybrid. Aquaculture 465:258–264

    Article  Google Scholar 

  • Chen N, Huang Z, Lu C, Shen Y, Luo X, Ke C, You W (2019) Different transcriptomic responses to thermal stress in heat-tolerant and heat-sensitive Pacific abalones indicated by cardiac performance. Front Physiol 9:1–14

    Google Scholar 

  • Choi MJ, Do Kim G, Kim JM, Lim HK (2015) Differentially-expressed genes associated with faster growth of the pacific abalone, Haliotis discus hannai. Int J Mol Sci 16:27520–27534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark MS, Peck LS (2009) Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna). Cell Stress Chaperones 14:649–660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark MS, Thorne MAS, Amaral A, Vieira F, Batista FM, Reis J, et al (2013) Identification of molecular and physiological responses to chronic environmental challenge in an invasive species: the Pacific oyster, Crassostrea gigas. Ecol Evol 3

  • Cook PA, Roy Gordon H (2010) World abalone supply, markets, and pricing. J Shellfish Res 29:569–571

    Article  Google Scholar 

  • Cox KW (1962) California abalones, family Haliotidae. Department of Fish and Game, the Resources Agency, State of California. Available at: https://books.google.com.mx/books?id=JgkMAQAAIAAJ

  • Crosson LM, Friedman CS (2018) Withering syndrome susceptibility of northeastern Pacific abalones: a complex relationship with phylogeny and thermal experience. J Invertebr Pathol 151:91–101

    Article  PubMed  Google Scholar 

  • Cunningham SC, Smith AM, Lamare MD (2016) The effects of elevated pCO2 on growth, shell production and metabolism of cultured juvenile abalone, Haliotis iris. Aquac Res 47:2375–2392

    Article  CAS  Google Scholar 

  • Dahlhoff E, Somero GN (1993) Effects of temperature on mitochondria from abalone (genus Haliotis) - adaptive plasticity and its limits. J Exp Biol 185:151–168

    Article  Google Scholar 

  • De Zoysa M, Whang I, Lee Y, Lee S, Lee J-S, Lee J (2009) Transcriptional analysis of antioxidant and immune defense genes in disk abalone (Haliotis discus discus) during thermal, low-salinity and hypoxic stress. Comp Biochem Physiol Part B Biochem Mol Biol 154:387–395

    Article  CAS  Google Scholar 

  • Desalvo MK, Sunagawa S, Voolstra CR, Medina M (2010) Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar Ecol Prog Ser 402:97–113

    Article  CAS  Google Scholar 

  • Detree C, Núñez-Acuña G, Roberts S, Gallardo-Escárate C (2016) Uncovering the complex transcriptome response of Mytilus chilensis against saxitoxin: implications of harmful algal blooms on mussel populations. PLoS One 11:e0165231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Díaz F, Del Río-Portílla MA, Sierra E, Aguilar M, Re-Araujo AD (2000) Preferred temperature and critical thermal maxima of red abalone Haliotis rufescens. J Therm Biol 25:257–261

    Article  Google Scholar 

  • Diaz F, Re AD, Medina Z, Re G, Valdez G, Valenzuela F (2006) Thermal preference and tolerance of green abalone Haliotis fulgens (Philippi, 1845) and pink abalone Haliotis corrugata (Gray, 1828). Aquac Res 37:877–884

    Article  Google Scholar 

  • Dickinson GH, Ivanina AV, Matoo OB, Portner HO, Lannig G, Bock C et al (2013) Interactive effects of elevated temperature and CO2 levels on metabolism and oxidative stress in two common marine bivalves (Crassostrea virginica and Mercenaria mercenaria). Comp Biochem Physiol A Mol Integr Physiol 164:545–553

    Article  CAS  Google Scholar 

  • Doncheva NT, Morris JH, Gorodkin J, Jensen LJ (2018) Cytoscape StringApp: network analysis and visualization of proteomics data. J Proteome Res 18:623–632

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elliott NG (2000) Genetic improvement programmes in abalone: what is the future? Aquac Res 31:51–59

    Article  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230

    Article  CAS  PubMed  Google Scholar 

  • Gavery MR, Roberts SB (2010) DNA methylation patterns provide insight into epigenetic regulation in the Pacific oyster (Crassostrea gigas). BMC Genomics 11:483

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gleason LU, Burton RS (2016) Genomic evidence for ecological divergence against a background of population homogeneity in the marine snail Chlorostoma funebralis. Mol Ecol 25:3557–3573

    Article  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo X, Yin H, Chen Y, Li L, Li J, Liu Q (2016) TAK1 regulates caspase 8 activation and necroptotic signaling via multiple cell death checkpoints. Cell Death Dis 7:1–11

    Google Scholar 

  • Huang WB, Ren HL, Gopalakrishnan S, Xu DD, Qiao K, Wang KJ (2010) First molecular cloning of a molluscan caspase from variously colored abalone (Haliotis diversicolor) and gene expression analysis with bacterial challenge. Fish Shellfish Immunol 28:587–595

  • Huang WB, Ren HL, Gopalakrishnan S, Xu DD, Qiao K, Wang KJ (2010) First molecular cloning of a molluscan caspase from variously colored abalone (Haliotis diversicolor) and gene expression analysis with bacterial challenge. Fish Shellfish Immunol 28:587–595

  • Juárez OE, Lafarga-De la Cruz F, Leyva-Valencia I, López-Landavery E, García-Esquivel Z, Díaz F et al (2018) Transcriptomic and metabolic response to chronic and acute thermal exposure of juvenile geoduck clams Panopea globosa. Mar Genomics 42:1–13

    Article  PubMed  Google Scholar 

  • Kültz D (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67:225–257

    Article  PubMed  CAS  Google Scholar 

  • Lafarga-De la Cruz F, Gallardo-Escárate C (2011) Intraspecies and interspecies hybrids in Haliotis: natural and experimental evidence and its impact on abalone aquaculture. Rev Aquac 3:74–99

    Article  Google Scholar 

  • Lafarga-De la Cruz F, Núñez-Acuña G, Gallardo-Escárate C (2013) Hybridization between Haliotis rufescens and Haliotis discus hannai: evaluation of fertilization, larval development, growth and thermal tolerance. Aquac Res 44:1206–1220

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leighton DL (1974) The influence of temperature on larval and juvenile growth in three species of Southern California abalones. Fish Bull 72:1137–1145

    Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang S, Luo X, You W, Luo L, Ke C (2014) The role of hybridization in improving the immune response and thermal tolerance of abalone. Fish Shellfish Immunol 39:69–77

  • Liang S, Luo X, You W, Ke C (2018) Hybridization improved bacteria resistance in abalone: evidence from physiological and molecular responses. Fish Shellfish Immunol 72:679–689

  • Maynard A, Bible JM, Pespeni MH, Sanford E, Evans TG (2018) Transcriptomic responses to extreme low salinity among locally adapted populations of Olympia oyster (Ostrea lurida). Mol Ecol 27:4225–4240

    Article  CAS  PubMed  Google Scholar 

  • Moore JD, Robbins TT, Friedman CS (2000) Withering syndrome in farmed red abalone Haliotis rufescens: thermal induction and association with a gastrointestinal Rickettsiales-like prokaryote. J Aquat Anim Health 12:26–34

    Article  PubMed  Google Scholar 

  • Morales-Bojorquez E, Orieta Mucino-Diaz M, Alfonso Velez-Barajas J (2008) Analysis of the decline of the abalone fishery (Haliotis fulgens and H. corrugata) along the westcentral coast of the Baja California peninsula, Mexico. J Shellfish Res 27:865–870

    Article  Google Scholar 

  • Morash AJ, Alter K (2016) Effects of environmental and farm stress on abalone physiology: perspectives for abalone aquaculture in the face of global climate change. Rev Aquac 8:342–368

    Article  Google Scholar 

  • 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–W185

    Article  PubMed  PubMed Central  Google Scholar 

  • Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, Furla P (2006) Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J 273:4186–4198

    Article  CAS  PubMed  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2009) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shiel BP, Hall NE, Cooke IR, Robinson NA, Strugnell JM (2017) Epipodial tentacle gene expression and predetermined resilience to summer mortality in the commercially important greenlip abalone, Haliotis laevigata. Mar Biotechnol 191–205:191–205

    Article  CAS  Google Scholar 

  • Sleight VA, Peck LS, Dyrynda EA, Smith VJ, Clark MS (2018) Cellular stress responses to chronic heat shock and shell damage in temperate Mya truncata. Cell Stress Chaperones 23:1003–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith-Unna R, Boursnell C, Patro R, Hibberd JM, Kelly S (2016) TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Res 26:1134–1144

  • Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53:597–608

    Article  PubMed  Google Scholar 

  • Somero, G. N. (2020). The cellular stress response and temperature: function, regulation and evolution. https://doi.org/10.1002/jez.2344

  • Sørensen JG, Loeschcke V (2007) Studying stress responses in the post-genomic era: its ecological and evolutionary role. J Biosci 32:447–456

    Article  PubMed  Google Scholar 

  • Storey KB (2004) Gene regulation in physiological stress. Int Congr Ser 1275:1–13

    Article  CAS  Google Scholar 

  • Tomanek L, Zuzow MJ, Ivanina AV, Beniash E, Sokolova IM (2011) Proteomic response to elevated PCO2 level in eastern oysters, Crassostrea virginica: evidence for oxidative stress. J Exp Biol 214:1836–1844

    Article  CAS  PubMed  Google Scholar 

  • Tripp-Valdez MA, Harms L, Pörtner HO, Sicard MT, Lucassen M (2019) De novo transcriptome assembly and gene expression profile of thermally challenged green abalone (Haliotis fulgens: Gastropoda) under acute hypoxia and hypercapnia. Mar Genomics 45:48–56

    Article  PubMed  Google Scholar 

  • Valenzuela-Miranda D, Del Río-Portilla MA, Gallardo-Escárate C (2015) Characterization of the growth-related transcriptome in California red abalone (Haliotis rufescens) through RNA-Seq analysis. Mar Genomics 24:199–202

    Article  PubMed  Google Scholar 

  • Vilchis LI, Tegner MJ, Moore JD, Friedman CS, Riser KL, Robbins TT, Dayton PK (2005) Ocean warming effects on growth, reproduction, and survivorship of Southern California abalone. Ecol Appl 15:469–480

    Article  Google Scholar 

  • Vosloo D, Vosloo A (2010) Response of cold-acclimated, farmed South African abalone (Haliotis midae) to short-term and long-term changes in temperature. J Therm Biol 35:317–323

    Article  Google Scholar 

  • Yan L, Su J, Wang Z, Yan X, Yu R, Ma P, Li Y, du J (2017) Transcriptomic analysis of Crassostrea sikamea × Crassostrea angulata hybrids in response to low salinity stress. PLoS One 12:e0171483

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang C, Gao Q, Liu C, Wang L, Zhou Z, Gong C, Zhang A, Zhang H, Qiu L, Song L (2017) The transcriptional response of the Pacific oyster Crassostrea gigas against acute heat stress. Fish Shellfish Immunol 68:132–143

    Article  CAS  PubMed  Google Scholar 

  • You WW, Ke CH, Luo X, Wang DX (2009) Growth and survival of three small abalone Haliotis diversicolor populations and their reciprocal crosses. Aquac Res 40:1474–1480

    Article  Google Scholar 

  • You W, Guo Q, Fan F, Ren P, Luo X, Ke C (2015) Experimental hybridization and genetic identification of Pacific abalone Haliotis discus hannai and green abalone H. fulgens. Aquaculture 448:243–249

    Article  CAS  Google Scholar 

  • Yu J, Liu F, Yin P, Zhao H, Luan W, Hou X, Zhong Y, Jia D, Zan J, Ma W, Shu B, Xu J (2013) Involvement of oxidative stress and mitogen-activated protein kinase signaling pathways in heat stress-induced injury in the rat small intestine. Stress 16:99–113

    Article  CAS  PubMed  Google Scholar 

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Code Availability

Code for RNAseq analysis is available as supplementary material.

Funding

The research was funded by the project SEP-CONACYT-CB-2014-238708. CONACYT provided the postdoctoral fellowships granted to MT and FC.

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Authors and Affiliations

  1. Departamento de Acuicultura, Centro de Investigación Científica y de Educación Superior de Ensenada, B. C. Carretera Tijuana-Ensenada 3918, Fraccionamiento Zona Playitas, 22860, Ensenada, Baja California, Mexico

    M. A. Tripp-Valdez, K. D. Chacón-Ponce & F. Lafarga-De la Cruz

  2. Departamento de Biotecnología Marina, Centro de Investigación Científica y de Educación Superior de Ensenada, B. C. Carretera Tijuana-Ensenada 3918, Fraccionamiento Zona Playitas, 22860, Ensenada, Baja California, Mexico

    F. Cicala, C. E. Galindo-Sánchez, E. López-Landavery, F. Díaz & D. Re-Araujo

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  1. M. A. Tripp-Valdez
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  2. F. Cicala
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  3. C. E. Galindo-Sánchez
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  6. F. Díaz
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Correspondence to F. Lafarga-De la Cruz.

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Electronic Supplementary Material

Supplementary material 1:

Differential Gene Expression analysis performed with EdgeR. (DOC 45 kb)

Supplementary material 2:

Seawater parameters of the header tanks during the 14-weeks incubation. (XLSX 11 kb)

Supplementary material 3:

Biweekly measurements of pure H. rufescens (RR) and hybrid (RP) abalone juveniles. (XLS 270 kb)

Supplementary material 4:

Raw reads outcome from the Illumina sequencing of pure H. rufescens (RR) and hybrid (RP) libraries. (XLS 29 kb)

Supplementary material 5:

Pathway enrichment performed with the KAAS annotation tool with the DET from the contrast RR18 vs RR22 and RP18 vs RP22. (XLSX 34 kb)

Supplementary material 6:

Transcript list from the DET related to the regulation of the immune response, regulation of the necroptotic process and pathways in cancer displayed in Fig. 6, including fold changes and FDR values. RRP18 denotes the contrast RR18 vs RP18; RRP22 denotes the contrast RR22 vs RP22; RR22 denotes the contrast RR18 vs RR22; RP22 denotes the contrast RP18 vs RP22. (XLS 25 kb)

Supplementary material 7:

Results of the functional enrichment analysis with TopGo of the down- and up-regulated annotated DET from pairwise contrast. RR indicates the pure H. rufescens while RP indicates hybrid abalone. (XLS 55 kb)

Supplementary material 8:

Transcript list from the DTE related to the oxidation reduction process displayed in Fig. 8, including fold changes and FDR values. RRP18 denotes the contrast RR18 vs RP18; RRP22 denotes the contrast RR22 vs RP22; RR22 denotes the contrast RR18 vs RR22; RP22 denotes the contrast RP18 vs RP22. (XLS 40 kb)

Supplementary material 9:

Transcript list from the DTE related to the growth, including fold changes and FDR values. RRP18 denotes the contrast RR18 vs RP18; RRP22 denotes the contrast RR22 vs RP22; RR22 denotes the contrast RR18 vs RR22; RP22 denotes the contrast RP18 vs RP22. (XLS 31 kb)

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Tripp-Valdez, M.A., Cicala, F., Galindo-Sánchez, C.E. et al. Growth Performance and Transcriptomic Response of Warm-Acclimated Hybrid Abalone Haliotis rufescens (♀) × H. corrugata (♂). Mar Biotechnol 23, 62–76 (2021). https://doi.org/10.1007/s10126-020-10002-7

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