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Comparative analysis of the cardiac structure and transcriptome of scallop and snail, perspectives on heart chamber evolution

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Abstract

The evolution of a two-chambered heart, with an atrium and a ventricle, has improved heart function in both deuterostomes (vertebrates) and some protostomes (invertebrates). Although studies have examined the unique structure and function of these two chambers, molecular comparisons are few and limited to vertebrates. Here, we focus on the two-chambered protostome heart of the mollusks, offering data that may provide a better understanding of heart evolution. Specifically, we asked if the atrium and ventricle differ at the molecular level in the mollusk heart. To do so, we examined two very different species, the giant African land snail (Lissachatina fulica) and the relatively small, aquatic yesso scallop (Mizuhopecten yessoensis), with the assumption that if they exhibited commonality these similarities would likely reflect those across the phylum. We found that, although the hearts of these two species differed histologically, their cardiac gene function enrichments were similar, as revealed by transcriptomic analysis. Furthermore, the atrium and ventricle in each species had distinct gene function clusters, suggesting an evolutionary differentiation of cardiac chambers in mollusks. Finally, to explore the relationship between vertebrate and invertebrate two-chambered hearts, we compared our transcriptomic data with published data from the zebrafish, a well-studied vertebrate model with a two-chambered heart. Our analysis indicated a functional similarity of ventricular genes between the mollusks and the zebrafish, suggesting that the ventricle was differentiated to achieve the same functions in invertebrates and vertebrates. As the first such study on protostomes, our findings offered initial insights into how the two-chambered heart arose, including a possible understanding of its occurrence in both protostomes and deuterostomes.

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Data availability

RNA-sequencing data are deposited in GEO under accession number GSE236112 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE236112).

References

  • Auman HJ, Coleman H, Riley HE, Olale F, Tsai HJ, Yelon D (2007) Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol 5:e53

    Article  PubMed  PubMed Central  Google Scholar 

  • Bettex DA, Pretre R, Chassot PG (2014) Is our heart a well-designed pump? The heart along animal evolution. Eur Heart J 35:2322–2332

    Article  PubMed  Google Scholar 

  • Bini G, Pugliese AM, Pepeu G, Chelazzi G (2006) Neuronal control of the cardiac responses to osmotic stress in the gastropod limpet Patella caerulea. J Exp Zool A Comp Exp Biol 305:472–479

    Article  PubMed  Google Scholar 

  • Boogerd CJ, Moorman AF, Barnett P (2009) Protein interactions at the heart of cardiac chamber formation. Ann Anat 191:505–517

    Article  CAS  PubMed  Google Scholar 

  • Buckett KJ, Peters M, Benjamin PR (1990) Excitation and inhibition of the heart of the snail, Lymnaea, by non-FMRFamidergic motoneurons. J Neurophysiol 63:1436–1447

    Article  CAS  PubMed  Google Scholar 

  • Burkhard S, van Eif V, Garric L, Christoffels VM, Bakkers J (2017) On the evolution of the cardiac pacemaker. J Cardiovasc Dev Dis 4:4

    PubMed  PubMed Central  Google Scholar 

  • Cao Y, Zhang X, Akerberg BN, Yuan H, Sakamoto T, Xiao F, VanDusen NJ, Zhou P, Sweat ME, Wang Y, Prondzynski M, Chen J, Zhang Y, Wang P, Kelly DP, Pu WT (2023) In vivo dissection of chamber-selective enhancers reveals estrogen-related receptor as a regulator of ventricular cardiomyocyte identity. Circulation 147:881–896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Luo W, Wang Y, Song X, Li S, Wu J, Sun L (2021) Directional homing of glycosylation-modified bone marrow mesenchymal stem cells for bone defect repair. J Nanobiotechnol 19:228

    Article  CAS  Google Scholar 

  • Collis LP, Sun Y, Hill RB (2006) Length-dependent deactivation of ventricular trabeculae in the bivalve, Spisula solidissima. J Comp Physiol B 176:371–385

    Article  CAS  PubMed  Google Scholar 

  • Darwin F (1876) On the structure of the snail’s heart. J Anat Physiol 10:506–510

    CAS  PubMed  PubMed Central  Google Scholar 

  • Davidson B (2007) Ciona intestinalis as a model for cardiac development. Semin Cell Dev Biol 18:16–26

    Article  CAS  PubMed  Google Scholar 

  • Dunn CW, Giribet G, Edgecombe GD, Hejnol A (2014) Animal phylogeny and its evolutionary implications. Annu Rev Ecol Evol Syst 45:371–395

    Article  Google Scholar 

  • Goodyer WR, Beyersdorf BM, Paik DT, Tian L, Li G, Buikema JW, Chirikian O, Choi S, Venkatraman S, Adams EL, Tessier-Lavigne M, Wu JC, Wu SM (2019) Transcriptomic profiling of the developing cardiac conduction system at single-cell resolution. Circ Res 125:379–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Y, Zhang Y, Liu Q, Huang Y, Mao G, Yue Z, Abe EM, Li J, Wu Z, Li S, Zhou X, Hu W, Xiao N (2019) A chromosomal-level genome assembly for the giant African snail Achatina fulica. Gigascience 8:1–8

    Article  CAS  Google Scholar 

  • Hernandez-Gea V, Camprecios G, Betancourt F, Perez-Campuzano V, Seijo S, Diaz A, Gallego-Duran R, Olivas P, Orts L, Magaz M, Baiges A, Turon F, Sidorova J, Romero-Gomez M, Lozano JJ, Garcia-Pagan JC (2021) Co-expression gene network analysis reveals novel regulatory pathways involved in porto-sinusoidal vascular disease. J Hepatol 75:924–934

    Article  CAS  PubMed  Google Scholar 

  • Huerta-Cepas J, Szklarczyk D, Heller D, Hernandez-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, von Mering C, Bork P (2019) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47:D309–D314

    Article  CAS  PubMed  Google Scholar 

  • Jin X, Li J, Li W, Wang X, Du C, Geng Z, Geng Y, Kang L, Zhang X, Wang M, Tian S (2020) Weighted gene co-expression network analysis reveals specific modules and biomarkers in Parkinson’s disease. Neurosci Lett 728:134950

    Article  CAS  PubMed  Google Scholar 

  • Katano W, Moriyama Y, Takeuchi JK, Koshiba-Takeuchi K (2019) Cardiac septation in heart development and evolution. Dev Growth Differ 61:114–123

    Article  PubMed  Google Scholar 

  • Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37:907–915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kodirov SA (2011) The neuronal control of cardiac functions in Molluscs. Comp Biochem Physiol A Mol Integr Physiol 160:102–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559

    Article  PubMed  PubMed Central  Google Scholar 

  • Liao Y, Smyth GK, Shi W (2014) FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930

    Article  CAS  PubMed  Google Scholar 

  • Litvinukova M, Talavera-Lopez C, Maatz H, Reichart D, Worth CL, Lindberg EL, Kanda M, Polanski K, Heinig M, Lee M, Nadelmann ER, Roberts K, Tuck L, Fasouli ES, DeLaughter DM, McDonough B, Wakimoto H, Gorham JM, Samari S, Mahbubani KT et al (2020) Cells of the adult human heart. Nature 588:466–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma H, Liu Z, Yang Y, Feng D, Dong Y, Garbutt TA, Hu Z, Wang L, Luan C, Cooper CD, Li Y, Welch JD, Qian L, Liu J (2021) Functional coordination of non-myocytes plays a key role in adult zebrafish heart regeneration. EMBO Rep 22:e52901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malyshev AY, Norekian TP, Balaban PM (2008) Neural control of heartbeat during two antagonistic behaviors: whole body withdrawal and escape swimming in the mollusk Clione limacina. J Comp Physiol A-Neuroethol Sens Neural Behav Physiol 194:899–906

    Article  PubMed  Google Scholar 

  • Marro J, Pfefferli C, de Preux Charles AS, Bise T, Jazwinska A (2016) Collagen XII contributes to epicardial and connective tissues in the zebrafish heart during ontogenesis and regeneration. PLoS One 11:e0165497

    Article  PubMed  PubMed Central  Google Scholar 

  • Martynova MG, Bystrova OA (2002) Undifferentiated cells in the snail myocardium are capable of DNA synthesis and myodifferentiation. Biol Bull 203:104–111

    Article  PubMed  Google Scholar 

  • Meyer M, Kircher M (2010) Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc 2010:pdb.prot5448

    Article  PubMed  Google Scholar 

  • Monahan-Earley R, Dvorak AM, Aird WC (2013) Evolutionary origins of the blood vascular system and endothelium. J Thromb Haemost 11:46–66

    Article  PubMed  PubMed Central  Google Scholar 

  • Moorman AF, Houweling AC, de Boer PA, Christoffels VM (2001) Sensitive nonradioactive detection of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol. J Histochem Cytochem 49:1–8

    Article  CAS  PubMed  Google Scholar 

  • North RJ (1963) The fine structure of the myofibers in the heart of the snail Helix aspersa. J Ultrastruct Res 8:206–218

    Article  CAS  PubMed  Google Scholar 

  • Ohata S, Kinoshita S, Aoki R, Tanaka H, Wada H, Tsuruoka-Kinoshita S, Tsuboi T, Watabe S, Okamoto H (2009) Neuroepithelial cells require fucosylated glycans to guide the migration of vagus motor neuron progenitors in the developing zebrafish hindbrain. Development 136:1653–1663

    Article  CAS  PubMed  Google Scholar 

  • Olejnickova V, Kolesova H, Bartos M, Sedmera D, Gregorovicova M (2022) The Tale-Tell Heart: evolutionary tetrapod shift from aquatic to terrestrial life-style reflected in heart changes in axolotl (Ambystoma mexicanum). Dev Dyn 251:1004–1014

    Article  CAS  PubMed  Google Scholar 

  • Pandolfo TJ, Cope WG, Arellano C (2009) Heart rate as a sublethal indicator of thermal stress in juvenile freshwater mussels. Comp Biochem Physiol A Mol Integr Physiol 154:347–352

    Article  PubMed  Google Scholar 

  • Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shumway SE, Parsons GJ (2016) Scallops: biology, ecology, aquaculture and fisheries, 3rd edn. Elsevier Science, Atlanta

    Google Scholar 

  • Singh AR, Sivadas A, Sabharwal A, Vellarikal SK, Jayarajan R, Verma A, Kapoor S, Joshi A, Scaria V, Sivasubbu S (2016) Chamber specific gene expression landscape of the zebrafish heart. PLoS ONE 11:e0147823

    Article  PubMed  PubMed Central  Google Scholar 

  • Tucker NR, Chaffin M, Fleming SJ, Hall AW, Parsons VA, Bedi KC Jr, Akkad AD, Herndon CN, Arduini A, Papangeli I, Roselli C, Aguet F, Choi SH, Ardlie KG, Babadi M, Margulies KB, Stegmann CM, Ellinor PT (2020) Transcriptional and cellular diversity of the human heart. Circulation 142:466–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Zhang J, Jiao W, Li J, Xun X, Sun Y, Guo X, Huan P, Dong B, Zhang L, Hu X, Sun X, Wang J, Zhao C, Wang Y, Wang D, Huang X, Wang R, Lv J, Li Y et al (2017) Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat Ecol Evol 1:120

    Article  PubMed  Google Scholar 

  • Weatherill D, Chase R (2005) Modulation of heart activity during withdrawal reflexes in the snail Helix aspersa. J Comp Physiol A-Neuroethol Sens Neural Behav Physiol 191:355–362

    Article  PubMed  Google Scholar 

  • Wells MJ, Smith PJS (1987) The performance of the octopus circulatory system: a triumph of engineering over design. Experientia 43:487–499

    Article  Google Scholar 

  • Wojciechowska A, Braniewska A, Kozar-Kaminska K (2017) MicroRNA in cardiovascular biology and disease. Adv Clin Exp Med 26:865–874

    Article  PubMed  Google Scholar 

  • Xavier-Neto J, Castro RA, Sampaio AC, Azambuja AP, Castillo HA, Cravo RM, Simoes-Costa MS (2007) Cardiovascular development: towards biomedical applicability. Cell Mol Life Sci 64:719–734

    Article  CAS  PubMed  Google Scholar 

  • Xing Q, Zhang L, Li Y, Zhu X, Li Y, Guo H, Bao Z, Wang S (2019) Development of novel cardiac indices and assessment of factors affecting cardiac activity in a bivalve mollusc Chlamys farreri. Front Physiol 10:293

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Q, Hao J, Gao F, Yang H (2019) Effect of temperature and thermal stress on the hemodynamics of the scallop Chlamys farreri, as indicated by Doppler ultrasonography. J Exp Mar Biol Ecol 510:1–9

    Article  CAS  Google Scholar 

  • Yang Z, Zhang L, Hu J, Wang J, Bao Z, Wang S (2020) The evo-devo of molluscs: insights from a genomic perspective. Evol Dev 22:409–424

    Article  PubMed  Google Scholar 

  • Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16:284–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Borikova AL, Ben-Yair R, Guner-Ataman B, MacRae CA, Lee RT, Burns CG, Burns CE (2014) Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc Natl Acad Sci USA 111:1403–1408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Ben-Yair R, Burns CE, Burns CG (2019) Endocardial notch signaling promotes cardiomyocyte proliferation in the regenerating zebrafish heart through Wnt pathway antagonism. Cell Rep 26:546-554.e5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Gao F, Gao S, Liang Y, Long H, Lv Z, Su Y, Ye N, Zhang L, Zhao C, Wang X, Song W, Zhang S, Dong B (2021) Biodiversity-based development and evolution: the emerging research systems in model and non-model organisms. Sci China Life Sci 64:1236–1280

    Article  PubMed  Google Scholar 

  • Zhou L, Liu Z, Dong Y, Sun X, Wu B, Yu T, Zheng Y, Yang A, Zhao Q, Zhao D (2019) Transcriptomics analysis revealing candidate genes and networks for sex differentiation of yesso scallop (Patinopecten yessoensis). BMC Genomics 20:671

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Dr. Qiang Xing (Ocean University of China, MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences) for providing scallops; Dr. Jing Wang (Ocean University of China, Fang Zongxi Centre for Marine EvoDevo & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences) for providing snails. This work was financially supported by Laoshan Laboratory (LSKJ202203204), the National Natural Science Foundation of China (31970506 and 32170541 to LZ; 31970475 and 32170832 to YS), and the Fundamental Research Funds for Central Universities, China (202012004 to LZ).

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Author notes

  1. Meina Lu, Rabia Hayat and Xuejiao Zhang have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, 266003, China

    Meina Lu, Rabia Hayat, Xuejiao Zhang, Yaqi Jiao, Ying Su & Long Zhao

  2. College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China

    Rabia Hayat, Yaqi Jiao, Shi Wang & Ying Su

  3. College of Fisheries, Ocean University of China, Qingdao, 266003, China

    Meina Lu, Xuejiao Zhang, Jianyun Huang, Yifan Huangfu, Mingcan Jiang, Jieyi Fu, Qingqiu Jiang, Yaojia Gu & Long Zhao

  4. Fang Zongxi Centre for Marine EvoDevo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China

    Shi Wang

  5. Division of Basic and Translational Cardiovascular Research, Department of Cardiology, Boston Children’s Hospital, Boston, MA, 02115, USA

    Alexander A. Akerberg

  6. Harvard Medical School, Boston, MA, 02115, USA

    Alexander A. Akerberg

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  1. Meina Lu
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Contributions

Conceptualization, YS and LZ; investigation, RH, ML, XZ, YJ, JH, YH, MJ, JF, QJ, and YG; Scallop genomics data, SW; transcriptomic analysis, ML; writing-original draft preparation, ML, XZ, and RH; writing-review and editing, AA, YS, and LZ; project administration, YS and LZ; funding acquisition, YS and LZ.

Corresponding authors

Correspondence to Ying Su or Long Zhao.

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Conflict of interest

The authors declare no conflicts of interest. Authors Long Zhao and Shi Wang are members of the Editorial Board, but they were not involved in the review of or decision related to this manuscript.

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No animal and human rights are involved in this article.

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Edited by Jiamei Li.

Special Topic: EvoDevo.

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Lu, M., Hayat, R., Zhang, X. et al. Comparative analysis of the cardiac structure and transcriptome of scallop and snail, perspectives on heart chamber evolution. Mar Life Sci Technol 5, 478–491 (2023). https://doi.org/10.1007/s42995-023-00202-0

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