AccScience Publishing / ESAM / Online First / DOI: 10.36922/ESAM025270017
ORIGINAL RESEARCH ARTICLE

Three-dimensional (3D) bioprinting of coral-polyp bio-skin using ultrashort and biofunctionalized peptide bioinks for transplantation on coral skeletons

Alexander U. Valle-Pérez1,2 Manola Moretti1,2 Panayiotis Bilalis1,2 Sebastian Overmans3 Kyle J. Lauersen3 Christian Baumgartner4 Charlotte A. E. Hauser1,2,4*
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1 Laboratory for Nanomedicine, Division of Biological and Environmental Science and Engineering (BESE), King Abdullah University of Science and Technology, Thuwal, Mecca Province, Kingdom of Saudi Arabia
2 Computational Bioscience Research Center (CBRC), King Abdullah University of Science and Technology, Thuwal, Mecca Province, Kingdom of Saudi Arabia
3 Laboratory for Sustainable & Synthetic Biotechnology, Division of Biological and Environmental Sciences and Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Mecca Province, Kingdom of Saudi Arabia
4 Institute of Health Care Engineering with European Testing Center of Medical Devices, Graz University of Technology (TU Graz), Graz, Styria, Austria
ESAM 2025, 1(3), 025270017 https://doi.org/10.36922/ESAM025270017
Received: 5 July 2025 | Revised: 12 August 2025 | Accepted: 19 August 2025 | Published online: 18 September 2025
© 2025 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Abstract

There is growing interest in applying 3D printing technologies to environmental restoration, particularly for fabricating bio-inspired artificial reefs and printing coral skeletons to attract fish and support coral growth and survival. More recently, tissue engineering and 3D bioprinting strategies have been employed to develop biomimetic biomaterials that more closely replicate the natural coral microenvironment, including the incorporation of coral symbionts, to aid restoration efforts. In this study, we investigate the use of diverse ultrashort peptide- and biofunctionalized peptide-based bioinks to support bail-out polyp re-settlement and subsequent micropropagation. Among the 13 bioinks examined, eight demonstrated polyp biocompatibility and stability under seawater conditions. We focused on two Scleractinia species, Stylophora pistillata and Pocillopora verrucosa, and optimized a culture strategy for microencapsulated bail-out polyps following re-settlement, comparing a single-entity versus clustered-entity approach. These advancements lay the groundwork for polyp transplantation using biomimetic biomaterials. The top-performing bioinks were selected based on bioink underwater stability, polyp biocompatibility, and suitability for 3D bioprinting of polyps onto coral skeletons. This led to the development of a coral-inspired, polyp-containing bio-skin graft designed to promote coral tissue regeneration. Here, we report the first results demonstrating the use of bioinks for coral polyp microencapsulation and 3D bioprinting with ultrashort peptide-based bioinks to support coral regeneration and transplantation on coral skeletons.

Keywords
3D bioprinting
Artificial coral tissue
Ultrashort peptide bioinks
Biofunctionalized bioinks
Coral polyp microencapsulation
Coral polyp transplantation
Polyp bail-out
Funding
This research was funded by King Abdullah University of Science and Technology (KAUST) to Charlotte A. E. Hauser. Additional funding was provided by Graz University of Technology (TU Graz) to Christian Baumgartner, and by research start-up funds awarded to Charlotte A. E. Hauser.
Conflict of interest
Charlotte A. E. Hauser is an Editorial Board Member of this journal, but was not in any way involved in the editorial and peer-review process conducted for this paper, directly or indirectly. Separately, other authors declared that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.
References
  1. Mieog JC, Van Oppen MJH, Berkelmans R, Stam WT, Olsen JL. Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real‐time PCR. Mol Ecol Resour. 2009;9(1):74-82. doi: 10.1111/j.1755-0998.2008.02222.x

 

  1. Silverstein RN, Correa AMS, Baker AC. Specificity is rarely absolute in coral-algal symbiosis: Implications for coral response to climate change. Proc R Soc B. 2012;279(1738):2609-2618. doi: 10.1098/rspb.2012.0055

 

  1. Sammarco P. Polyp Bail-Out: An escape response to environmental stress and a new means of reproduction in corals. Mar Ecol Prog Ser. 1982;10:57-65. doi: 10.3354/meps010057

 

  1. Serrano E, Coma R, Inostroza K, Serrano O. Polyp bail-out by the coral Astroides calycularis (Scleractinia, Dendrophylliidae). Mar Biodiv. 2018;48(3):1661-1665. doi: 10.1007/s12526-017-0647-x

 

  1. Cardoso PM, Alsaggaf AA, Villela HM, Peixoto RS. Inducing polyp bail-out in coral colonies to obtain individualized micropropagates for laboratory experimental use. J Vis Exp. 2022;(182):63840. doi: 10.3791/63840

 

  1. Shapiro OH, Kramarsky-Winter E, Gavish AR, Stocker R, Vardi A. A coral-on-a-chip microfluidic platform enabling live-imaging microscopy of reef-building corals. Nat Commun. 2016;7(1):10860. doi: 10.1038/ncomms10860

 

  1. Pang AP, Luo Y, He C, Lu Z, Lu X. A polyp-on-chip for coral long-term culture. Sci Rep. 2020;10(1):6964. doi: 10.1038/s41598-020-63829-4

 

  1. Chuang PS, Ishikawa K, Mitarai S. Morphological and genetic recovery of coral polyps after bail-out. Front Mar Sci. 2021;8:609287. doi: 10.3389/fmars.2021.609287

 

  1. Hauser CAE, Deng R, Mishra A, et al. Natural tri- to hexapeptides self-assemble in water to amyloid β-type fiber aggregates by unexpected α-helical intermediate structures. Proc Natl Acad Sci USA. 2011;108(4):1361-1366. doi: 10.1073/pnas.1014796108

 

  1. Roger LM, Lewinski NA, Putnam HM, Roxbury D, Tresguerres M, Wangpraseurt D. Nanobiotech engineering for future coral reefs. One Earth. 2023;6(7):778-789. doi: 10.1016/j.oneear.2023.05.008

 

  1. Susapto HH, Alhattab D, Abdelrahman S, et al. Ultrashort peptide bioinks support automated printing of large-scale constructs assuring long-term survival of printed tissue constructs. Nano Lett. 2021;21(7):2719-2729. doi: 10.1021/acs.nanolett.0c04426

 

  1. Tóth GS, Backman O, Siivola T, et al. Employing photocurable biopolymers to engineer photosynthetic 3D-printed living materials for production of chemicals. Green Chem. 2024;26(7):4032-4042. doi: 10.1039/D3GC04264B

 

  1. Wangpraseurt D, You S, Azam F, et al. Bionic 3D printed corals. Nat Commun. 2020;11(1):1748. doi: 10.1038/s41467-020-15486-4

 

  1. Wangpraseurt D, Sun Y, You S, et al. Bioprinted living coral microenvironments mimicking coral‐algal symbiosis. Adv Funct Mater. 2022;32(35):2202273. doi: 10.1002/adfm.202202273

 

  1. Roger L, Lewinski N, Putnam H, et al. Nanotechnology for coral reef conservation, restoration and rehabilitation. Nat Nanotechnol. 2023;18(8):831-833. doi: 10.1038/s41565-023-01402-6

 

  1. de León EHP, Valle-Pérez AU, Khan ZN, Hauser CAE. Intelligent and smart biomaterials for sustainable 3D printing applications. Curr Opin Biomed Eng. 2023;26:100450. doi: 10.1016/j.cobme.2023.100450

 

  1. Zhao S, Guo C, Kumarasena A, Omenetto FG, Kaplan DL. 3D printing of functional microalgal silk structures for environmental applications. ACS Biomater Sci Eng. 2019;5(9):4808-4816. doi: 10.1021/acsbiomaterials.9b00554

 

  1. Krujatz F, Lode A, Brüggemeier S, et al. Green bioprinting: Viability and growth analysis of microalgae immobilized in 3D‐plotted hydrogels versus suspension cultures. Eng Life Sci. 2015;15(7):678-688. doi: 10.1002/elsc.201400131

 

  1. Wangpraseurt D, You S, Sun Y, Chen S. Biomimetic 3D living materials powered by microorganisms. Trends Biotechnol. 2022;40(7):843-857. doi: 10.1016/j.tibtech.2022.01.003

 

  1. Valenzuela Matus I, Góis J, Vaz-Pires P, Lino Alves J. Coral propagation in substrates obtained through additive manufacturing: Influence of mortar formulations on seawater parameters. ACS Sustain Chem Eng. 2024;12(37):13721- 13740. doi: 10.1021/acssuschemeng.4c01276

 

  1. Levy N, Kundu S, Freckelton M, et al. Microbial living materials promote coral larval settlement. PNAS Nexus. 2025;4(9):pgaf268. doi: 10.1093/pnasnexus/pgaf268

 

  1. Contardi M, Fadda M, Isa V, et al. Biodegradable Zein-based biocomposite films for underwater delivery of curcumin reduce thermal stress effects in corals. ACS Appl Mater Interfaces. 2023;15(28):33916-33931. doi: 10.1021/acsami.3c01166

 

  1. Luo C, Li M, Yuan R, Yang Y, Lu Z, Ge L. Biocompatible self-healing coating based on schiff base for promoting adhesion of coral cells. ACS Appl Bio Mater. 2020;3(3):1481-1495. doi: 10.1021/acsabm.9b01113

 

  1. Roger LM, Adarkwa Darko Y, Bernas T, et al. Evaluation of fluorescence-based viability stains in cells dissociated from scleractinian coral Pocillopora damicornis. Sci Rep. 2022;12(1):15297. doi: 10.1038/s41598-022-19586-7

 

  1. Baker NR. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu Rev Plant Biol. 2008;59(1):89-113. doi: 10.1146/annurev.arplant.59.032607.092759

 

  1. Overmans S, Ignacz G, Beke AK, et al. Continuous extraction and concentration of secreted metabolites from engineered microbes using membrane technology. Green Chem. 2022;24(14):5479-5489. doi: 10.1039/D2GC00938B

 

  1. Khan Z, Kahin K, Hauser C. Time-dependent pulsing of microfluidic pumps to enhance 3D bioprinting of peptide bioinks. In: Gray BL, Becker H, editors. Microfluidics, BioMEMS, and Medical Microsystems XIX. Washington, DC: SPIE; 2021. p. 5. doi: 10.1117/12.2578830

 

  1. Rauf S, Susapto HH, Kahin K, et al. Self-assembling tetrameric peptides allow in situ 3D bioprinting under physiological conditions. J Mater Chem B. 2021;9(4): 1069-1081. doi: 10.1039/D0TB02424D

 

  1. Unal AZ, West JL. Synthetic ECM: Bioactive synthetic hydrogels for 3D tissue engineering. Bioconjugate Chem. 2020;31(10):2253-2271. doi: 10.1021/acs.bioconjchem.0c00270

 

  1. Bilalis P, Alrashoudi AΑ, Susapto HH, et al. Dipeptide-based photoreactive instant glue for environmental and biomedical applications. ACS Appl Mater Interfaces. 2023;15(40): 46710-46720. doi: 10.1021/acsami.3c10726

 

  1. Jia Y, Abdelrahman S, Hauser CAE. Developing a sustainable resin for 3D printing in coral restoration. MSAM. 2024;3(2):3125. doi: 10.36922/msam.3125

 

  1. Albalawi HI, Khan ZN, Valle-Pérez AU, et al. Sustainable and eco-friendly coral restoration through 3D printing and fabrication. ACS Sustain Chem Eng. 2021;9(37): 12634-12645. doi: 10.1021/acssuschemeng.1c04148

 

  1. Do TD, LaPointe NE, Economou NJ, et al. Effects of pH and charge state on peptide assembly: The YVIFL model system. J Phys Chem B. 2013;117(37):10759-10768. doi: 10.1021/jp406066d

 

  1. Hopkins E, Sanvictores T, Sharma S. Physiology, Acid Base Balance. Treasure Island, FL: StatPearls Publishing; 2024.

 

  1. Abdelmongy A, El-Moselhy K. Seasonal variations of the physical and chemical properties of seawater at the Northern Red Sea, Egypt. Open J Ocean Coastal Sci. 2015;2(1):1-17. doi: 10.15764/OCS.2015.01001

 

  1. Rasul NMA, Stewart ICF, editors. Oceanographic and Biological Aspects of the Red Sea. Berlin: Springer International Publishing; 2019. doi: 10.1007/978-3-319-99417-8

 

  1. Hauser CAE, Zhang S. Designer self-assembling peptide nanofiber biological materials. Chem Soc Rev. 2010;39(8):2780. doi: 10.1039/b921448h

 

  1. Zhao X, Pan F, Xu H, et al. Molecular self-assembly and applications of designer peptide amphiphiles. Chem Soc Rev. 2010;39(9):3480. doi: 10.1039/b915923c

 

  1. Chan KH, Lee WH, Ni M, Loo Y, Hauser CAE. C-terminal residue of ultrashort peptides impacts on molecular self-assembly, hydrogelation, and interaction with small-molecule drugs. Sci Rep. 2018;8(1):17127. doi: 10.1038/s41598-018-35431-2

 

  1. Haerianardakani S, Kreutzer AG, Salveson PJ, Samdin TD, Guaglianone GE, Nowick JS. Phenylalanine mutation to cyclohexylalanine facilitates triangular trimer formation by β-hairpins derived from Aβ. J Am Chem Soc. 2020;142(49):20708-20716. doi: 10.1021/jacs.0c09281

 

  1. Brower DL, Brower SM, Hayward DC, Ball EE. Molecular evolution of integrins: Genes encoding integrin β subunits from a coral and a sponge. Proc Natl Acad Sci USA. 1997;94(17):9182-9187. doi: 10.1073/pnas.94.17.9182

 

  1. Iguchi A, Márquez LM, Knack B, et al. Apparent involvement of a β1 type integrin in coral fertilization. Mar Biotechnol. 2007;9(6):760-765. doi: 10.1007/s10126-007-9026-0

 

  1. Jones VAS, Dorr M, Siemers I, et al. Symbiont-specific uptake is mediated by integrins in cnidarian larvae. bioRxiv. 2025. doi: 10.1101/2025.01.21.633834

 

  1. Levy S, Elek A, Grau-Bové X, et al. A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity. Cell. 2021; 184(11):2973-2987.e18. doi: 10.1016/j.cell.2021.04.005

 

  1. Mao X, Nie Y, Huang Y, Ji H, Li X. A radial distribution of calices in coral skeleton of Pocillopora verrucosa (Ellis and Solander, 1786) against ocean currents. Mar Biol. 2021;168(12):171. doi: 10.1007/s00227-021-03982-0

 

  1. Xu J, Pérez-Pedroza R, Moretti M, et al. 3D bioprinting of colon organoids in ultrashort self-assembling and decorated peptide matrices. IJB. 2024;0(0):3033. doi: 10.36922/ijb.3033

 

  1. Su T, Liu Y, He H, et al. Strong bioinspired polymer hydrogel with tunable stiffness and toughness for mimicking the extracellular matrix. ACS Macro Lett. 2016;5(11):1217-1221. doi: 10.1021/acsmacrolett.6b00702

 

  1. Trappmann B, Chen CS. How cells sense extracellular matrix stiffness: A material’s perspective. Curr Opin Biotechnol. 2013;24(5):948-953. doi: 10.1016/j.copbio.2013.03.020

 

  1. Wen JH, Vincent LG, Fuhrmann A, et al. Interplay of matrix stiffness and protein tethering in stem cell differentiation. Nat Mater. 2014;13(10):979-987. doi: 10.1038/nmat4051

 

  1. Wiedenmann J, D’Angelo C, Mardones ML, et al. Reef-building corals farm and feed on their photosynthetic symbionts. Nature. 2023;620(7976):1018-1024. doi: 10.1038/s41586-023-06442-5

 

  1. Weis VM. Corals have algal friends for dinner. Nature. 2023;620(7976):951-952. doi: 10.1038/d41586-023-02593-7

 

  1. Avila-Ramírez A, Valle-Pérez AU, Susapto HH, et al. Ecologically friendly biofunctional ink for reconstruction of rigid living systems under wet conditions. Int J Bioprint. 2021;7(4):398. doi: 10.18063/ijb.v7i4.398
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