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Estrogen induces shift in abundances of specific groups of the coral microbiome

  • 1.

    Ghiselli, G. & Jardim, W. F. Interferentes endócrinos no meio ambiente. Quím. Nova 30, 695–706 (2007).

    Article  Google Scholar 

  • 2.

    Vilela, C. L. S., Bassin, J. P. & Peixoto, R. S. Water contamination by endocrine disruptors: Impacts, microbiological aspects and trends for environmental protection. Environ. Poll. 235, 546–559 (2018).

    CAS  Article  Google Scholar 

  • 3.

    Muller, M. et al. Occurrence of estrogens in sewage sludge and their fate during plant-scale anaerobic digestion. Chemosphere 81, 65–71 (2010).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 4.

    Mills, M. R. et al. Removal of ecotoxicity of 17α-ethinylestradiol using TAML/peroxide water treatment. Sci. Rep. 5, 1–10 (2015).

    Article  CAS  Google Scholar 

  • 5.

    Laurenson, J. P., Bloom, R. A., Page, S. & Sadrieh, N. Ethinylestradiol and other human pharmaceutical estrogens in the aquatic environment: A review of recent risk assessment data. AAPS J. 16, 299–310 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 6.

    Luzio, A., Santos, D., Fontaínhas-Fernandes, A. A., Monteiro, S. M. & Coimbra, A. M. Effects of 17α-ethinylestradiol at different water temperatures on zebrafish sex differentiation and gonad development. Aquat. Toxicol. 174, 22–35 (2016).

    CAS  PubMed  Article  Google Scholar 

  • 7.

    Blewett, T., MacLatchy, D. L. & Wood, C. M. The effects of temperature and salinity on 17-α-ethynylestradiol uptake and its relationship to oxygen consumption in the model euryhaline teleost (Fundulus heteroclitus). Aquat. Toxicol. 127, 61–71 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 8.

    Atkinson, S., Atkinson, M. J. & Tarrant, A. M. Estrogens from sewage in coastal marine environments. Environ. Health Persp. 111, 531–535 (2003).

    CAS  Article  Google Scholar 

  • 9.

    Segner, H. et al. Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: Report from the European IDEA project. Ecotoxicol. Environ. Safe. 54, 302–314 (2003).

    CAS  Article  Google Scholar 

  • 10.

    Tyler, C. R., Jobling, S. & Sumpter, J. P. Endocrine disruption in wildlife: A critical review of the evidence. Crit. Rev. Toxicol. 28, 319–361 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 11.

    Johnson, A. C., Belfroid, A. & Di Corcia, A. Estimating steroid oestrogen inputs into activated sludge treatment works and observations on their removal from the effluent. Sci. Total Environ. 256, 163–173 (2000).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 12.

    Cadwell, D. J. et al. Derivation of an aquatic predicted no-effect concentration for the synthetic hormone, 17α-ethinyl estradiol. Environ. Sci. Technol. 10, 272–283 (2008).

    Google Scholar 

  • 13.

    Ternes, T. A. et al. Behavior and occurrence of estrogens in municipal sewage treatment plants—I. Investigations in Germany, Canada and Brazil. Sci. Total Environ. 225, 81–90 (1999).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 14.

    Kolpin, D. W. et al. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: A national reconnaissance. Environ. Sci. Technol. 36, 1202–1211 (2002).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 15.

    Huang, Y., Wang, X. L., Zhang, J. W. & Wu, K. S. Impact of endocrine-disrupting chemicals on reproductive function in zebrafish (Danio rerio). Reprod. Domest. Anim. 50, 1–6 (2009).

    Article  CAS  Google Scholar 

  • 16.

    Länge, R. et al. Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 20, 1216–1227 (2001).

    PubMed  Article  PubMed Central  Google Scholar 

  • 17.

    Parrott, J. L. & Blunt, B. R. Life-cycle exposure of fathead minnows (Pimephales promelas) to an ethinylestradiol concentration below 1 ng/L reduces egg fertilization success and demasculinizes males. Environ. Toxicol. 20, 131–141 (2005).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 18.

    Bloom, M. S., Micu, R. & Neamtiu, I. Female infertility and “emerging” organic pollutants of concern. Curr. Epidemiol. Rep. 3, 39–50. https://doi.org/10.1007/s40471-016-0060-1 (2016).

    Article  Google Scholar 

  • 19.

    Nash, J. P. et al. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Persp. 112, 1725–1733 (2004).

    CAS  Article  Google Scholar 

  • 20.

    Wu, C., Huang, X., Lin, J. & Liu, J. Occurrence and fate of selected endocrine-disrupting chemicals in water and sediment from an urban lake. Arch. Environ. Contam. Toxicol. 68, 225–236 (2014).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 21.

    Pennington, M. J. et al. Effects of contaminants of emerging concern on Megaselia scalaris (Lowe, Diptera: Phoridae) and its microbial community. Sci. Rep. 7, 1–12 (2017).

    CAS  Article  Google Scholar 

  • 22.

    Pennington, M. J., Prager, S. M., Walton, W. E. & Trumble, J. T. Culex quinquefasciatus larval microbiomes vary with instar and exposure to common wastewater contaminants. Sci. Rep. 6, 1–9 (2016).

    Article  CAS  Google Scholar 

  • 23.

    Pennington, M. J., Rivas, N. G., Prager, S. M., Walton, W. E. & Trumble, J. T. Pharmaceuticals and personal care products alter the holobiome and development of a medically important mosquito. Environ. Pollut. 203, 199–207 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 24.

    Fosch, S. E. et al. Contraception: Influence on vaginal microbiota and identification of vaginal lactobacilli using MALDI-TOF MS and 16S rDNA sequencing. Open Microbiol. J. 12, 218–229 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 25.

    Tarrant, A. M., Blomquist, C. H., Lima, P. H., Atkinson, M. J. & Atkinson, S. Metabolism of estrogens and androgens by scleractinian corals. Comp. Biochem. Phys. B. 136, 473–485 (2003).

    Article  CAS  Google Scholar 

  • 26.

    Tarrant, A. M., Atkinson, M. J. & Atkinson, S. Effects of steroidal estrogens on coral growth and reproduction. Mar. Ecol. Prog. Ser. 269, 121–129 (2004).

    ADS  CAS  Article  Google Scholar 

  • 27.

    Atkinson, S. & Atkinson, M. J. Detection of estradiol-17β during a mass coral spawn. Coral Reefs 11, 33–35 (1992).

    ADS  Article  Google Scholar 

  • 28.

    Atkinson, S. Uptake of estrone from the water column by a coral community. Mar. Biol. 139, 321–325 (2001).

    Article  Google Scholar 

  • 29.

    Rougée, L. R., Richmond, R. H. & Collier, A. C. Molecular reproductive characteristics of the reef coral Pocillopora damicornis. Comp. Biochem. Phys. A 189, 38–44 (2015).

    Article  CAS  Google Scholar 

  • 30.

    Blomquist, C. H., Lima, P. H., Tarrant, A. M., Atkinson, M. J. & Atkinson, S. 17β-Hydroxysteroid dehydrogenase (17β-HSD) in scleractinian corals and zooxanthellae. Comp. Biochem. Phys. B 143, 397–403 (2006).

    Article  CAS  Google Scholar 

  • 31.

    Tarrant, A. M., Atkinson, S. & Atkinson, M. J. Estrone and estradiol-17β concentration in tissue of the scleractinian coral, Montipora verrucosa. Comp. Biochem. Phys. A 122, 85–92 (1999).

    CAS  Article  Google Scholar 

  • 32.

    Twan, W. et al. Hormones and reproduction in scleractinian corals. Comp. Biochem. Phys. A 144, 247–253 (2006).

    Article  CAS  Google Scholar 

  • 33.

    Tarrant, A., Atkinson, M. & Atkinson, S. Uptake of estrone from the water column by a coral community. Mar. Biol. 139, 321–325 (2001).

    CAS  Article  Google Scholar 

  • 34.

    Bosch, T. C. G. & McFall-Ngai, M. J. Metaorganisms as the new frontier. Zoology 114, 185–190 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 35.

    Rosenberg, E., Koren, O., Reshef, L. & Efrony, R. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355–362 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 36.

    Rosenberg, E. Coral microbiology. Microb. Biotechnol. 2, 147 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  • 37.

    Peixoto, R. S., Rosado, P. M., Leite, D. C., Rosado, A. S. & Bourne, D. G. Beneficial microorganisms for corals (BMC): Proposed mechanisms for coral health and resilience. Front. Mar. Sci. 8, 1–16 (2017).

    CAS  Google Scholar 

  • 38.

    Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Patterns of coral heat tolerance. Nature Comm. 1, 1–8 (2017).

    Google Scholar 

  • 39.

    Peixoto, R. S., Sweet, M. & Bourne, D. G. Customized medicine for corals. Front. Mar. Sci. 6, 686 (2019).

    Article  Google Scholar 

  • 40.

    Rosado, P. M. et al. Marine probiotics: Increasing coral resistance to bleaching through microbiome manipulation. ISME J. 13, 921–936 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 41.

    Lesser, M. P., Mazel, C. H., Gorbunov, M. Y. & Falkowski, P. G. Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305, 997–1000 (2004).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 42.

    Wegley, L., Edwards, R., Rodriguez-Brito, B., Liu, H. & Rohwer, F. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9, 2707–2719 (2007).

    CAS  PubMed  Article  Google Scholar 

  • 43.

    Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 8, 2068–2073 (2006).

    CAS  PubMed  Article  Google Scholar 

  • 44.

    Ritchie, K. B. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322, 1–14 (2006).

    ADS  CAS  Article  Google Scholar 

  • 45.

    Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: Underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340 (2016).

    CAS  PubMed  Article  Google Scholar 

  • 46.

    Santos, H. F. et al. Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J. 8, 2272–2279 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 47.

    Santos, H. F. et al. Impact of oil spills on coral reefs can be reduced by bioremediation using probiotic microbiota. Sci. Rep. 5, 1–11 (2015).

    Google Scholar 

  • 48.

    Röthig, T., Yum, L. K., Kremb, S. G., Roik, A. & Voolstra, C. R. Microbial community composition of deep-sea corals from the Red Sea provides insight into functional adaption to a unique environment. Sci. Rep. 7, 44714 (2017).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 49.

    Meyer, J. L., Paul, V. J. & Teplitski, M. Community shifts in the surface microbiomes of the coral Porites astreoides with unusual lesions. PLoS ONE 9, e100316 (2014).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 50.

    Sweet, M. J. & Bulling, M. T. On the importance of the microbiome and pathobiome in coral health and disease. Front. Mar. Sci. 4, 1–11 (2017).

    Article  Google Scholar 

  • 51.

    Grottoli, A. G. et al. Coral physiology and microbiome dynamics under combined warming and ocean acidification. PLoS ONE 13, e0191156 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 52.

    Webster, N. S. et al. Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. Rep. 6, 19324 (2016).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 53.

    Ainsworth, T. D., Thurber, R. V. & Gates, R. D. The future of coral reefs: A microbial perspective. Trends Ecol. Evol. 25, 233–240 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  • 54.

    Gissi, F. et al. The effect of dissolved nickel and copper on the adult coral Acropora muricata and its microbiome. Environ. Pollut. 250, 792–806 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 55.

    Leite, D. C. et al. Coral bacterial-core abundance and network complexity as proxies for anthropogenic pollution. Front. Microbiol. 9, 833 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 56.

    Vega Thurber, R. et al. Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 11, 2148–2163 (2009).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 57.

    Meron, D. et al. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 5, 51–60 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 58.

    McDevitt-Irwin, J. M., Baum, J. K., Garren, M. & Vega Thurber, R. L. Responses of coral-associated bacterial communities to local and global stressors. Front. Mar. Sci. 4, 262 (2017).

    Article  Google Scholar 

  • 59.

    Al-Dahash, L. M. & Mahmoud, H. M. Harboring oil-degrading bacteria: A potential mechanism of adaptation and survival in corals inhabiting oil-contaminated reefs. Mar. Pollut. Bull. 72, 364–374 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 60.

    Wenger, A. S., Fabricius, K. E., Jones, G. P. & Brodie, J. E. Effects of sedimentation, eutrophication, and chemical pollution on coral reef fishes. In Ecology of Fishes on Coral Reefs (ed. Mora, C.) 145–153 (Cambridge University Press, Cambridge, 2015).

    Google Scholar 

  • 61.

    Zaneveld, J. R. et al. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat. Commun. 7, 1–12 (2016).

    Article  CAS  Google Scholar 

  • 62.

    Marangoni, L. F. et al. Copper effects on biomarkers associated with photosynthesis, oxidative status and calcification in the Brazilian coral Mussismilia harttii (Scleractinia, Mussidae). Mar. Environ. Res. 130, 248–257 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 63.

    Ferrigno, F. et al. Corals in high diversity reefs resist human impact. Ecol. Indic. 70, 106–113 (2016).

    Article  Google Scholar 

  • 64.

    Hughes, T. P. et al. Climate change, human impacts, and the resilience of coral reefs. Science 80, 929–933 (2003).

    ADS  Article  CAS  Google Scholar 

  • 65.

    Pastorok, R. & Bilyard, G. Effects of sewage pollution on coral-reef communities. Mar. Ecol. Prog. Ser. 21, 175–189 (1985).

    ADS  Article  Google Scholar 

  • 66.

    Tarrant, A. M. Hormonal signaling in cnidarians: Do we understand the pathways well enough to know whether they are being disrupted?. Ecotoxicology 16, 5–13 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 67.

    Peters, E. C., Gassman, N. J., Firman, J. C., Richmond, R. H. & Power, E. A. Ecotoxicology of tropical marine ecosystems. Environ. Toxicol. Chem. 16, 12–40 (1997).

    CAS  Article  Google Scholar 

  • 68.

    Holert, J. et al. Metagenomes reveal global distribution of bacterial steroid catabolism in natural, engineered, and host environments. MBio 9, e02345-e2417 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 69.

    Winter, A. P. M., Chaloub, R. M. & Duarte, G. A. S. Photosynthetic responses of corals Mussismilia harttii (Verrill, 1867) from turbid waters to changes in temperature and presence/absence of light. Braz. J. Oceanogr. 64, 203–216 (2016).

    Article  Google Scholar 

  • 70.

    Fonseca, J. S., Marangoni, L. F. B., Marques, J. A. & Bianchini, A. Effects of increasing temperature alone and combined with copper exposure on biochemical and physiological parameters in the zooxanthellate scleractinian coral Mussismilia harttii. Aquat. Toxicol. 190, 121–132 (2017).

    CAS  PubMed  Article  Google Scholar 

  • 71.

    Ralph, P. J., Schreiber, U., Gademann, R., Kühl, M. & Larkum, A. W. D. Coral photobiology studied with a new imaging pulse amplitude modulated fluorometer. J. Phycol. 41, 335–342 (2005).

    Article  Google Scholar 

  • 72.

    Sato, Y., Bourne, D. G. & Willis, B. L. Effects of temperature and light on the progression of black band disease on the reef coral, Montiporahispida. Coral Reefs 30, 753–761 (2011).

    ADS  Article  Google Scholar 

  • 73.

    Wiedenmann, J. et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 160–164 (2013).

    ADS  CAS  Article  Google Scholar 

  • 74.

    Fernando, S. C. et al. Microbiota of the major south atlantic reef building. Microb. Ecol. 69, 267–280 (2015).

    PubMed  Article  Google Scholar 

  • 75.

    De Castro, A. P., Dias, S. A. & Reis, A. M. M. Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from eastern Brazil. Microb. Ecol. 59, 658–667 (2010).

    PubMed  Article  Google Scholar 

  • 76.

    Santos, H. F. et al. Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: Bacterial proxies for oil pollution. PLoS ONE 6, e14693 (2011).

    Article  CAS  Google Scholar 

  • 77.

    Santos, H. F., Cury, J. C., Carmo, F. L., Rosado, A. S. & Peixoto, R. S. 18S rDNA sequences from microeukaryotes reveal oil indicators in mangrove sediment. PLoS ONE 5, e12437 (2010).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 78.

    Oleynik, G. N., Yurishinets, V. I. & Starosila, Y. V. Bacterioplankton and bacteriobenthos as biological indicators of the aquatic ecosystems’ state (a review). Hydrobiol. J. 47, 37–48 (2011).

    Article  Google Scholar 

  • 79.

    Jain, A., Singh, B. N., Singh, S. P., Singh, H. B. & Singh, S. Exploring biodiversity as bioindicators for water pollution. Natl. Conf. Biodivers. Dev. Poverty Alleviation, 50–56 (2010).

  • 80.

    Bloem, J. & Breure, A. M. Microbial indicators. In Bioindicators and Biomonitors (eds Markert, B. A. et al.) 257–282 (Elsevier, Amsterdam, 2003).

    Google Scholar 

  • 81.

    Parmar, T. K., Rawtani, D. & Agrawal, Y. K. Bioindicators: The natural indicator of environmental pollution. Front. Life Sci. 9, 110–118 (2016).

    CAS  Article  Google Scholar 

  • 82.

    Wilkins, L. G. E. et al. Host-associated microbiomes drive structure and function of marine ecosystems. PLoS Biol. 17, e3000533 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 83.

    Kurisu, F., Ogura, M., Saitoh, S., Yamazoe, A. & Yagi, O. Degradation of natural estrogen and identification of the metabolites produced by soil isolates of Rhodococcus sp. and Sphingomonas sp.. J. Biosci. Bioeng. 109, 576–582 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 84.

    Wang, Y. et al. Degradation of 17 β-estradiol and products by a mixed culture of Rhodococcus equi DSSKP-R-001 and Comamonas testosteroni QYY20150409. Biotechnol. Biotechnol. Equip. 33, 268–277 (2019).

    CAS  Article  Google Scholar 

  • 85.

    Yoshimoto, T. et al. Isolates from activated sludge in wastewater treatment plants. Appl. Environ. Microbiol. 70, 5283–5289 (2004).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 86.

    Zhao, H. et al. Genome analysis of Rhodococcus sp. DSSKP-R-001: A highly effective β-estradiol-degrading bacterium. Int. J. Genomics 2018, 3505428 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 87.

    Edet, U. O. & Antai, S. P. Correlation and distribution of xenobiotics genes and metabolic activities with level of total petroleum hydrocarbon in soil, sediment and estuary water in the Niger Delta Region of Nigeria. Asian J. Biotechnol. Genet. Eng. 1(1), 1–11 (2018).

    Google Scholar 

  • 88.

    Parida, S. & Sharma, D. The microbiome-estrogen connection and breast cancer risk. Cells 8, 1642 (2019).

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 89.

    Schreiber, U. Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: An overview. In Chlorophyll a Fluorescence: A Signature of Photosynthesis (eds Papageorgiou, G. C. & Govindjee, C.) 279–319 (Springer, Berlin, 2004).

    Google Scholar 

  • 90.

    Siebeck, U. E., Marshall, N. J., Klüter, A. & Hoegh-Guldberg, O. Monitoring coral bleaching using a colour reference card. Coral Reefs 25, 453–460 (2006).

    ADS  Article  Google Scholar 

  • 91.

    Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST: Paleontological statistics software package. Palaeontol. Electron. 4, 1–9 (2001).

    Google Scholar 

  • 92.

    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. U.S.A. 108, 4516–4522 (2011).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 93.

    Schloss, P. D. et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 94.

    McCune, B. & Mefford, M. J. PC-ORD v. 6.0. MjM Software, Gleneden Beach (2010).


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