Skip to main content
SpringerLink
Log in

Visualisation of Phosphate in Subcalicoblastic Extracellular Calcifying Medium and on a Skeleton of Coral by Using a Novel Probe, Fluorescein-4-Isothiocyanate-Labelled Alendronic Acid

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The overload of nutrients of anthropogenic origin, including phosphate, onto coastal waters has been reported to have detrimental effects on corals. However, to the best of our knowledge, the phosphate concentration threshold for inhibiting coral calcification is unclear owing to a lack of information on the molecular mechanisms involved in the inhibitory effect of phosphate. Therefore, in this study, we prepared a new phosphate analogue, fluorescein-4-isothiocyanate (FITC)-labelled alendronic acid (FITC-AA), from commercially available reagents and used it as a novel probe to demonstrate its transfer pathway from ambient seawater into Acropora digitifera. When the juveniles at 1 d post-settlement were treated with FITC-AA in a laboratory tank, this phosphate analogue was found in the subcalicoblastic extracellular calcifying medium (SCM) and was absorbed on the basal plate in the juveniles within a few minutes. When the juveniles bear zooxanthellae at 3 months post-settlement, FITC-AA was observed on the corallite walls within a few minutes after adding ambient seawater. We concluded that FITC-AA in ambient seawater was transferred via a paracellular pathway to SCM and then absorbed on the coral CaCO3 skeletons because FITC-AA with a high polarity group cannot permeate through cell membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aihara Y, Maruyama S, Baird AH, Iguchi A, Takahashi S, Minagawa J (2019) Green fluorescence from cnidarian hosts attract symbiotic algae. Proc Natl Acad Sci U S A 116:2118–2123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allemand D, Tambutté É, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, p 119–150, Coral Calcification, Cells to Reefs

  • Bell PR, Lapointe BE, Elmetri I (2007) Reevaluation of ENCORE: support for the eutrophication threshold model for coral reefs. AMBIO J Hum Environ 36:416–424.

  • Burke L, Reytar K, Spalding M, Perry A (2011) In reefs at risk revisited. World Resources Institute, Washington, DC

    Google Scholar 

  • Demes KW, Bell SS, Dawes CJ (2009) The effects of phosphate on the biomineralisation of the green alga, Halimeda incrassata (Ellis) lam. J Exp Mar Biol Ecol 374:123–127.

  • Dunn JG, Sammarco PW, LaFleur G (2012) Effects of phosphate on growth and skeletal density in the scleractinian coral Acropora muricata: a controlled experimental approach. J Exp Mar Biol Ecol 411:34–44.

  • Houk P, Comeros-Raynal M, Lawrence A, Sudek M, Vaeoso M, McGuire K, Regis J (2020) Nutrient thresholds to protect water quality and coral reefs. Mar Pollut Bull 159:111451.

  • Iijima M, Yasumoto J, Iguchi A, Koiso K, Ushigome S, Nakajima N, Kunieda Y, Nakamura T, Sakai K, Yasumoto-Hirose M, Mori-Yasumoto K, Mizusawa N, Amano H, Suzuki A, Jimbo M, Watabe S, Yasumoto K (2021) Phosphate bound to calcareous sediments hampers skeletal development of juvenile coral. R Soc Open Sci 8:201214.

  • Iijima M, Yasumoto K, Yasumoto J, Yasumoto-Hirose M, Kuniya N, Takeuchi R, Nozaki M, Nanba N, Nakamura T, Jimbo M, Watabe S (2019) Phosphate enrichment hampers the development of juvenile Acropora digitifera coral by inhibiting skeleton formation. Mar Biotechnol (NY) 21:291–300.

  • Iwao K, Fujisawa T, Hatta M (2002) A cnidarian neuropeptide of the GLWamide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reefs 21:127–129.

  • Koop K, Booth D, Broadbent A, Brodie J, Bucher D, Capone D, Coll J, Dennison W, Erdmann M, Harrison P, Hoegh-Guldberg O, Hutchings P, Jones GB, Larkum AW, O’Neil J, Steven A, Tentori E, Ward S, Williamson J, Yellowlees D (2001) ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar Pollut Bull 42:91–120.

  • Le Goff C, Tambutté E, Venn AA, Techer N, Allemand D, Tambutté S (2017) In vivo pH measurement at the site of calcification in an octocoral. Sci Rep 7:11210.

  • Millero F, Huang F, Zhu X, Liu X, Zhang JZ (2001) Adsorption and desorption of phosphate on calcite and aragonite in seawater. Aquat Geochem 7:33–56.

  • Norat-Ramírez J, Méndez-Lázaro P, Hernández-Delgado EA, Mattei-Torres H, Cordero-Rivera L (2019) A septic waste index model to measure the impact of septic tanks on coastal water quality and coral reef communities in Rincon, Puerto Rico. Ocean Coast Manag 169:201–213.

  • Ohno Y, Iguchi A, Shinzato C, Gushi M, Inoue M, Suzuki A, Sakai K, Nakamura T (2017a) Calcification process dynamics in coral primary polyps as observed using a calcein incubation method. Biochem Biophys Rep 9:289–294.

  • Ohno Y, Iguchi A, Shinzato C, Inoue M, Suzuki A, Sakai K, Nakamura T (2017b) An aposymbiotic primary coral polyp counteracts acidification by active pH regulation. Sci Rep 7:40324.

  • Rott E, Steinmetz H, Metzger JW (2018) Organophosphonates: a review on environmental relevance, biodegradability and removal in wastewater treatment plants. Sci Total Environ 615:1176–1191.

  • Sawada K, Abdel-Aal N, Sekino H, Satoh K (2003) Adsorption of inorganic phosphates and organic polyphosphonate on calcite. Dalton Trans 3:342–347.

  • Suzuki T, Inomata S, Sawada K (1986) Adsorption of phosphate on calcite. J Chem Soc Faraday Trans 1:1733–1743.

  • Tambutté E, Tambutté S, Segonds N, Zoccola D, Venn A, Erez J, Allemand D (2012) Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. Proc Biol Sci 279:19–27.

  • Tisthammer KH, Timmins-Schiffman E, Seneca FO, Nunn BL, Richmond RH (2021) Physiological and molecular responses of lobe coral indicate nearshore adaptations to anthropogenic stressors. Sci Rep 11:3423.

  • Weston SA, Parish CR (1992) Calcein: a novel marker for lymphocytes which enter lymph nodes. Cytometry:J. Int Soc Anal Cytol 13:739–749.

  • Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret FE, Postle AD, Achterberg EP (2013) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nature Clim Change 3:160–164.

  • Wolff NH, Mumby PJ, Devlin M, Anthony KRN (2018) Vulnerability of the Great Barrier Reef to climate change and local pressures. Glob Chang Biol 24:1978–1991.

  • Yamashiro H (1995) The effects of HEBP, an inhibitor of mineral deposition, upon photosynthesis and calcification in the scleractinian coral, Stylophora pistillata. J Exp Mar Biol Ecol 191:57–63.

Download references

Acknowledgements

This research was supported by the Environment Research and Technology Development Fund (JPMEERF20194007) of the Environmental Restoration and Conservation Agency of Japan and by Grants-in-Aid from the Japan Society for the Promotion of Science (KAKENHI Grant Numbers 19K12310 and 20H03077), Research Laboratory on Environmentally-conscious Developments and Technologies (E-code) at the National Institute of Advanced Industrial Science and Technology (AIST), and by a Grant-in-Aid for Research Fellow of Japan Society for the Promotion of Science Grant Number 21J01671.

Author information

Authors and Affiliations

  1. National Institute of Advanced Industrial Science and Technology (AIST), AIST Tsukuba Central 7, 1-1-1 Higashi, Tsukuba, Ibaraki, 305-8567, Japan

    Mariko Iijima, Akira Iguchi & Atsushi Suzuki

  2. Kitasato University School of Marine Biosciences, 1-15-1 Kitasato, Minami, Sagamihara, Kanagawa, 252-0373, Japan

    Mariko Iijima, Nanami Mizusawa, Mitsuru Jimbo, Shugo Watabe & Ko Yasumoto

  3. Faculty of Agriculture, University of the Ryukyus, 1 Senbaru, Nishihara, Nakagusuku, Okinawa, 903-0213, Japan

    Jun Yasumoto

  4. Faculty of Pharmaceutical Sciences, Tokyo University of Science, Noda, Chiba, 278-8510, Japan

    Kanami Mori-Yasumoto

  5. Tropical Technology Plus, 12-75 Suzaki, Uruma, Okinawa, 904-2234, Japan

    Mina Yasumoto-Hirose

  6. Research Laboratory On Environmentally-Conscious Developments and Technologies [E-Code], National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, 305-8567, Japan

    Akira Iguchi & Atsushi Suzuki

Authors
  1. Mariko Iijima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Yasumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kanami Mori-Yasumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mina Yasumoto-Hirose
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Akira Iguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Atsushi Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nanami Mizusawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mitsuru Jimbo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shugo Watabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ko Yasumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MI and KY conceived and designed the study; MI, JY, AI, and MY-H collected juvenile corals; KM-Y analysed the chemical structure; NM, AS, MJ, and SW coordinated the study and helped draft the manuscript. All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Corresponding author

Correspondence to Ko Yasumoto.

Ethics declarations

Ethics Approval

We have been allowed to harvest corals by Okinawa Prefectural Permits (numbers: 30–32, 31–43).

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 391 KB)

Supplementary file2 (MP4 23599 KB)

Supplementary file3 (MP4 1153 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iijima, M., Yasumoto, J., Mori-Yasumoto, K. et al. Visualisation of Phosphate in Subcalicoblastic Extracellular Calcifying Medium and on a Skeleton of Coral by Using a Novel Probe, Fluorescein-4-Isothiocyanate-Labelled Alendronic Acid. Mar Biotechnol 24, 524–530 (2022). https://doi.org/10.1007/s10126-022-10115-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-022-10115-1

Keywords

Search

Navigation