Histology and transcriptomic analyses of barnacles with different base materials and habitats shed lights on the duplication and chemical diversification of barnacle cement proteins
Tóm tắt
Barnacles are sessile crustaceans that attach to underwater surfaces using barnacle cement proteins. Barnacles have a calcareous or chitinous membranous base, and their substratum varies from biotic (e.g. corals/sponges) to abiotic surfaces. In this study, we tested the hypothesis that the cement protein (CP) composition and chemical properties of different species vary according to the attachment substrate and/or the basal structure. We examined the histological structure of cement glands and explored the variations in cement protein homologs of 12 barnacle species with different attachment habitats and base materials. Cement gland cells in the rocky shore barnacles Tetraclita japonica formosana and Amphibalanus amphitrite are eosinophilic, while others are basophilic. Transcriptome analyses recovered CP homologs from all species except the scleractinian coral barnacle Galkinia sp. A phylogenomic analysis based on sequences of CP homologs did not reflect a clear phylogenetic pattern in attachment substrates. In some species, certain CPs have a remarkable number of paralogous sequences, suggesting that major duplication events occurred in CP genes. The examined CPs across taxa show consistent bias toward particular sets of amino acid. However, the predicted isoelectric point (pI) and hydropathy are highly divergent. In some species, conserved regions are highly repetitive. Instead of developing specific cement proteins for different attachment substrata, barnacles attached to different substrata rely on a highly duplicated cementation genetic toolkit to generate paralogous CP sequences with diverse chemical and biochemical properties. This general CP cocktail might be the key genetic feature enabling barnacles to adapt to a wide variety of substrata.
Tài liệu tham khảo
Chan BKK, Høeg JT. Diversity of lifestyles, sexual systems, and larval development patterns in sessile crustaceans. In: Thiel M, Watling L, editor. Lifestyles and Feeding Biology, The Natural History of the Crustacea, vol. 2. New York: Oxford University Press; 2015. pp. 14–34.
Yu M-C, Dreyer N, Kolbasov GA, Høeg JT, Chan BKK. Sponge symbiosis is facilitated by adaptive evolution of larval sensory and attachment structures in barnacles. Proceedings of the Royal Society B. 2020; 287(1927):20200300.
Dreyer N, Zardus JD, Høeg JT, Olesen J, Yu M-C, Chan BKK. How whale and dolphin barnacles attach to their hosts and the paradox of remarkably versatile attachment structures in cypris larvae. Org Divers Evol. 2020; 20(2):233–249.
Fitridge I, Dempster T, Guenther J, De Nys R. The impact and control of biofouling in marine aquaculture: a review. Biofouling. 2012; 28(7):649–669.
Waiho K, Glenner H, Miroliubov A, Noever C, Hassan M, Ikhwanuddin M et al. Rhizocephalans and their potential impact on crustacean aquaculture. Aquaculture. 2020:735876.
Aldred N, Alsaab A, Clare AS. Quantitative analysis of the complete larval settlement process confirms Crisp’s model of surface selectivity by barnacles. Proceedings of the Royal Society B: Biological Sciences. 2018; 285(1872):20171957.
Liang C, Strickland J, Ye Z, Wu W, Hu B, Rittschof D. Biochemistry of barnacle adhesion: an updated review. Frontiers in Marine Science. 2019; 6:565.
Høeg JT, Maruzzo D, Okano K, Glenner H, Chan BKK. Metamorphosis in balanomorphan, pedunculated, and parasitic barnacles: a video-based analysis. Integr Comp Biol. 2012; 52(3):337–347.
Yule AB, Walker G. Settlement of Balanus balanoides: The effect of cyprid antennular secretion. J Mar Biol Assoc U K. 1985; 65(3):707–712.
Aldred N, Clare AS. Mechanisms and principles underlying temporary adhesion, surface exploration and settlement site selection by barnacle cyprids: a short review. In: Gorb SN, editor. Functional surfaces in biology, vol. 2. Dordrecht: Springer Netherlands; 2009. pp. 43–65.
Power AM, Klepal W, Zheden V, Jonker J, McEvilly P, von Byern J. Mechanisms of Adhesion in Adult Barnacles. In: Byern J, Grunwald I, editor. Biological Adhesive Systems. Vienna: Springer; 2010. pp. 153–168.
Kamino K. Barnacle underwater attachment. In: Smith A, Callow J, editor. Biological Adhesives. Berlin, Heidelberg: Springer; 2006. pp. 145–166.
Cheung P, Ruggieri G, Nigrelli R. A new method for obtaining barnacle cement in the liquid state for polymerization studies. Mar Biol. 1977; 43(2):157–163.
Chan BKK, Prabowo RE, Lee K-S. Crustacean Fauna of Taiwan: Barnacles, Volume I - Cirripedia: Thoracica excluding the Pyrgomatidae and Acastinae, vol. 1. Keelung: National Taiwan Ocean University; 2009.
Chan BKK, Chen Y-Y, Achituv Y. Crustacean Fauna of Taiwan: Barnacles, Volume II - Cirripedia: Thoracica: Pyrgomatidae, vol. 2. Taipei, Taiwan: Biodiversity Research Center, Academia Sinica; 2013.
Yu M-C, Kolbasov GA, Høeg JT, Chan BKK. Crustacean-sponge symbiosis: collecting and maintaining sponge-inhabiting barnacles (Cirripedia: Thoracica: Acastinae) for studies on host specificity and larval biology. J Crustacean Biol. 2019; 39(4):522–532.
Lacombe D. A comparative study of the cement glands in some balanid barnacles (Cirripedia, Balanidae). Biol Bull. 1970; 139(1):164–179.
Lacombe D, Liguori VR. Comparative histological studies of the cement apparatus of Lepas anatifera and Balanus tintinnabulum. Biol Bull. 1969; 137(1):170–180.
Lobo-da-Cunha A, Alves Â, Oliveira E, Cunha I. The cement apparatus of the stalked barnacle Pollicipes pollicipes. Mar Biol. 2017; 164:11.
Saroyan J, Lindner E, Dooley C. Repair and reattachment in the Balanidae as related to their cementing mechanism. Biol Bull. 1970; 139(2):333–350.
Otness JS, Medcalf DG. Chemical and physical characterization of barnacle cement. Comp Biochem Physiol B Comp Biochem. 1972; 43(2):443–449.
Walker G. The biochemical composition of the cement of two barnacle species, Balanus hameri and Balanus crenatus. J Mar Biol Assoc U K. 1972; 52(2):429–435.
Kamino K, Odo S, Maruyama T. Cement proteins of the acorn-barnacle, Megabalanus rosa. Biol Bull. 1996; 190(3):403–409.
Naldrett MJ, Kaplan DL. Characterization of barnacle (Balanus eburneus and B. cenatus) adhesive proteins. Mar Biol. 1997; 127(4):629–635.
Kamino K, Inoue K, Maruyama T, Takamatsu N, Harayama S, Shizuri Y. Barnacle cement proteins: importance of disulfide bonds in their insolubility. J Biol Chem. 2000; 275(35):27360–27365.
Khandeparker L, Anil AC. Underwater adhesion: The barnacle way. Int J Adhesion Adhes. 2007; 27(2):165–172.
So CR, Fears KP, Leary DH, Scancella JM, Wang Z, Liu JL et al. Sequence basis of barnacle cement nanostructure is defined by proteins with silk homology. Sci Rep. 2016; 6:36219
Liu JCW, Høeg JT, Chan BKK. How do coral barnacles start their life in their hosts? Biol Lett. 2016; 12(6):20160124.
Jonker J-L, Morrison L, Lynch EP, Grunwald I, von Byern J, Power AM. The chemistry of stalked barnacle adhesive (Lepas anatifera). Interface focus. 2015; 5:20140062.
Jonker J-L, Abram F, Pires E, Coelho AV, Grunwald I, Power AM. Adhesive proteins of stalked and acorn barnacles display homology with low sequence similarities. PLoS ONE. 2014; 9(10):e108902.
Lin H-C, Wong YH, Tsang LM, Chu KH, Qian P-Y, Chan BKK. First study on gene expression of cement proteins and potential adhesion-related genes of a membranous-based barnacle as revealed from Next-Generation Sequencing technology. Biofouling. 2014; 30(2):169–181.
Domínguez-Pérez D, Almeida D, Wissing J, Machado AM, Jänsch L, Castro LF et al. The quantitative proteome of the cement and adhesive gland of the pedunculate barnacle, Pollicipes pollicipes. Int J Mol Sci. 2020; 21(7):2524.
Rocha M, Antas P, Castro LFC, Campos A, Vasconcelos V, Pereira F et al. Comparative analysis of the adhesive proteins of the adult stalked goose barnacle Pollicipes pollicipes (Cirripedia: Pedunculata). Mar Biotechnol. 2019; 21(1):38–51.
Zheden V, Klepal W, von Byern J, Bogner FR, Thiel K, Kowalik T et al. Biochemical analyses of the cement float of the goose barnacle Dosima fascicularis–a preliminary study. Biofouling. 2014; 30(8):949–963.
Machado AM, Sarropoulou E, Castro LFC, Vasconcelos V, Cunha I. An important resource for understanding bio-adhesion mechanisms: Cement gland transcriptomes of two goose barnacles, Pollicipes pollicipes and Lepas anatifera (Cirripedia, Thoracica). Marine Genomics. 2019; 45:16–20.
Chan BKK, Dreyer N, Gale AS, Glenner H, Ewers-Saucedo C, Pérez-Losada M, Kolbasov GA, Crandall JA, Høeg JT. The evolutionary diversity of barnacles, with an updated classification of fossil and living forms. Zool. J. Linn. Soc. 2021; zlaa160. https://doi.org/10.1093/zoolinnean/zlaa160.
Wang Z, Leary DH, Liu J, Settlage RE, Fears KP, North SH et al. Molt-dependent transcriptomic analysis of cement proteins in the barnacle Amphibalanus amphitrite. BMC Genomics. 2015; 16:859.
So CR, Scancella JM, Fears KP, Essock-Burns T, Haynes SE, Leary DH et al. Oxidase Activity of the Barnacle Adhesive Interface Involves Peroxide-Dependent Catechol Oxidase and Lysyl Oxidase Enzymes. ACS Appl Mater Interfaces. 2017; 9(13):11493–11505.
Remm M, Storm CE, Sonnhammer EL. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol. 2001; 314(5):1041–1052.
Luo H, Nijveen H. Understanding and identifying amino acid repeats. Brief Bioinform. 2014; 15(4):582–591.
Knebelmann B, Deschenes G, Gros F, Hors M, Grünfeld J, Zhou J et al. Substitution of arginine for glycine 325 in the collagen alpha 5 (IV) chain associated with X-linked Alport syndrome: characterization of the mutation by direct sequencing of PCR-amplified lymphoblast cDNA fragments. American journal of human genetics. 1992; 51(1):135–142.
Gatesy J, Hayashi C, Motriuk D, Woods J, Lewis R. Extreme diversity, conservation, and convergence of spider silk fibroin sequences. Science. 2001; 291(5513):2603–2605.
Jung H, Pena-Francesch A, Saadat A, Sebastian A, Kim DH, Hamilton RF et al. Molecular tandem repeat strategy for elucidating mechanical properties of high-strength proteins. Proc Natl Acad Sci USA. 2016; 113(23):6478–6483.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30(15):2114–2120.
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013; 8(8):1494–1512.
Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10(3):R25.
Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12:323.
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12):550.
Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017; 14(4):417–419.
Kim J-H, Kim H, Kim H, Chan BKK, Kang S, Kim W. Draft genome assembly of a fouling barnacle, Amphibalanus amphitrite (Darwin, 1854): the first reference genome for Thecostraca. Front Ecol Evol. 2019; 7:465.
Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015; 12(1):59–60.
Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019; 20(1):238.
Lan Y, Sun J, Tian R, Bartlett DH, Li R, Wong YH et al. Molecular adaptation in the world’s deepest-living animal: Insights from transcriptome sequencing of the hadal amphipod Hirondellea gigas. Mol Ecol. 2017; 26(14):3732–3743.
Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016; 33(7):1870–1874.
Pagès HA, Gentleman P, DebRoy S. Biostrings: Efficient manipulation of biological strings. R package version 2.56.0; 2020.
Kozlowski LP. IPC - Isoelectric Point Calculator. Biol Direct. 2016; 11(55):16.
Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006; 34(suppl_2):W369-W373.