Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals
Abstract
:1. Introduction
2. Materials and Methods
2.1. Experimental Setup and Sampling
2.2. DNA Extraction, 16S Library Preparation, Sequencing
2.3. Data Processing
2.4. Statistical Analyses
2.5. Shared ASVs
2.6. Water Nutrient Analysis
3. Results
3.1. Environmental Conditions Significantly Varied over 8-Week Experimental Period
3.2. Corals Have Increased Sensitivity to Nutrient Enrichment Compared to Their Resident Fish and Algal Matrix
3.3. Between Sample Diversity Changed Significantly for Each Host
3.4. Coral Microbiomes Are Dominated by One Bacterial Genus While Fish and Algae Microbiomes Are More Even
3.5. Fish and Algae Microbiomes Had Several Taxa Significantly Varying in Abundance over Time
3.6. Despite a Strong Trophic Interaction Few Microbes Are Shared among the Three Hosts
4. Discussion
4.1. Coral Microbiomes Respond Uniquely to Nutrient Enrichment
4.2. Cryptic Environmental and/or Biological Factors May Be Altering Fish and Algal Matrix Microbiomes
4.3. Shared ASVs Indicate Microbial Transmission Amongst Members of This Trophic Symbiosis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Stock, C.A.; Powell, T.M.; Levin, S.A. Bottom–up and Top–down Forcing in a Simple Size-Structured Plankton Dynamics Model. J. Mar. Syst. 2008, 74, 134–152. [Google Scholar] [CrossRef]
- Williams, I.; Polunin, N. Large-Scale Associations between Macroalgal Cover and Grazer Biomass on Mid-Depth Reefs in the Caribbean. Coral Reefs 2001, 19, 358–366. [Google Scholar] [CrossRef]
- Friedlander, A.; Brown, E.; Monaco, M. Defining Reef Fish Habitat Utilization Patterns in Hawaii: Comparisons between Marine Protected Areas and Areas Open to Fishing. Mar. Ecol.-Prog. Ser. 2007, 351, 221–233. [Google Scholar] [CrossRef] [Green Version]
- Tebbett, S.B.; Goatley, C.H.R.; Bellwood, D.R. The Effects of Algal Turf Sediments and Organic Loads on Feeding by Coral Reef Surgeonfishes. PLoS ONE 2017, 12, e0169479. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, J.E.; Brainard, R.; Carter, A.; Grillo, S.; Edwards, C.; Harris, J.; Lewis, L.; Obura, D.; Rohwer, F.; Sala, E.; et al. Re-Evaluating the Health of Coral Reef Communities: Baselines and Evidence for Human Impacts across the Central Pacific. Proc. R. Soc. B Biol. Sci. 2016, 283, 20151985. [Google Scholar] [CrossRef] [PubMed]
- Burkepile, D.E.; Hay, M.E. Herbivore vs. Nutrient Control of Marine Primary Producers: Context-Dependent Effects. Ecology 2006, 87, 3128–3139. [Google Scholar] [CrossRef] [Green Version]
- Hughes, T.P.; Rodrigues, M.J.; Bellwood, D.R.; Ceccarelli, D.; Hoegh-Guldberg, O.; McCook, L.; Moltschaniwskyj, N.; Pratchett, M.S.; Steneck, R.S.; Willis, B. Phase Shifts, Herbivory, and the Resilience of Coral Reefs to Climate Change. Curr. Biol. 2007, 17, 360–365. [Google Scholar] [CrossRef] [Green Version]
- Bellwood, D.R.; Pratchett, M.S.; Morrison, T.H.; Gurney, G.G.; Hughes, T.P.; Álvarez-Romero, J.G.; Day, J.C.; Grantham, R.; Grech, A.; Hoey, A.S.; et al. Coral Reef Conservation in the Anthropocene: Confronting Spatial Mismatches and Prioritizing Functions. Biol. Conserv. 2019, 236, 604–615. [Google Scholar] [CrossRef]
- Tebbett, S.B.; Bellwood, D.R. Algal Turf Sediments on Coral Reefs: What’s Known and What’s Next. Mar. Pollut. Bull. 2019, 149, 110542. [Google Scholar] [CrossRef]
- Casey, J.M.; Ainsworth, T.D.; Choat, J.H.; Connolly, S.R. Farming Behaviour of Reef Fishes Increases the Prevalence of Coral Disease Associated Microbes and Black Band Disease. Proc. R. Soc. B Biol. Sci. 2014, 281, 20141032. [Google Scholar] [CrossRef]
- Gobler, C.; Gutierrez, D.; Davis, T.; Peterson, B.; Liddle, L. Algal Assemblages Associated with Stegastes Sp. Territories on Indo-Pacific Coral Reefs: Characterization of Diversity and Controls on Growth. J. Exp. Mar. Biol. Ecol. 2006, 336, 135–145. [Google Scholar] [CrossRef]
- Johnson, M.K.; Holbrook, S.J.; Schmitt, R.J.; Brooks, A.J. Fish Communities on Staghorn Coral: Effects of Habitat Characteristics and Resident Farmerfishes. Environ. Biol. Fish 2011, 91, 429–448. [Google Scholar] [CrossRef]
- Wilson, S.; Bellwood, D.; Choat, J.; Furnas, M. Detritus in the Epilithic Algal Matrix and Its Use by Coral Reef Fishes. Oceanogr. Mar. Biol. Annu. Rev. 2003, 41, 279–309. [Google Scholar]
- Wilson, S.; Bellwood, D.R. Cryptic Dietary Components of Territorial Damselfishes (Pomacentridae, Labroidei). Mar. Ecol. Prog. Ser. 1997, 153, 299–310. [Google Scholar] [CrossRef] [Green Version]
- Birrell, C.L.; McCook, L.J.; Willis, B.L. Effects of Algal Turfs and Sediment on Coral Settlement. Mar. Pollut. Bull. 2005, 51, 408–414. [Google Scholar] [CrossRef]
- Vermeij, M.J.A.; Smith, J.E.; Smith, C.M.; Vega Thurber, R.; Sandin, S.A. Survival and Settlement Success of Coral Planulae: Independent and Synergistic Effects of Macroalgae and Microbes. Oecologia 2009, 159, 325–336. [Google Scholar] [CrossRef]
- Birrell, C.; Mccook, L.; Willis, B.; Diaz-Pulido, G. Effects of Benthic Algae on the Replenishment of Corals and the Implications for the Resilience of Coral Reefs. Oceanogr. Mar. Biol. 2008, 46, 25–51. [Google Scholar]
- River, G.F.; Edmunds, P.J. Mechanisms of Interaction between Macroalgae and Scleractinians on a Coral Reef in Jamaica. J. Exp. Mar. Biol. Ecol. 2001, 261, 159–172. [Google Scholar] [CrossRef]
- Titlyanov, E.A.; Yakovleva, I.M.; Titlyanova, T.V. Interaction between Benthic Algae (Lyngbya Bouillonii, Dictyota Dichotoma) and Scleractinian Coral Porites Lutea in Direct Contact. J. Exp. Mar. Biol. Ecol. 2007, 342, 282–291. [Google Scholar] [CrossRef]
- Barott, K.L.; Rodriguez-Mueller, B.; Youle, M.; Marhaver, K.L.; Vermeij, M.J.A.; Smith, J.E.; Rohwer, F.L. Microbial to Reef Scale Interactions between the Reef-Building Coral Montastraea Annularis and Benthic Algae. Proc. R. Soc. B Biol. Sci. 2012, 279, 1655–1664. [Google Scholar] [CrossRef] [Green Version]
- Barott, K.; Smith, J.; Dinsdale, E.; Hatay, M.; Sandin, S.; Rohwer, F. Hyperspectral and Physiological Analyses of Coral-Algal Interactions. PLoS ONE 2009, 4, e8043. [Google Scholar] [CrossRef]
- Haas, A.; El-Zibdah, M.; Wild, C. Seasonal Monitoring of Coral–Algae Interactions in Fringing Reefs of the Gulf of Aqaba, Northern Red Sea. Coral Reefs 2010, 29, 93–103. [Google Scholar] [CrossRef]
- Casey, J.; Connolly, S.; Ainsworth, T. Coral Transplantation Triggers Shift in Microbiome and Promotion of Coral Disease Associated Potential Pathogens. Sci. Rep. 2015, 5, 11903. [Google Scholar] [CrossRef] [PubMed]
- Blanchette, A.; Ely, T.; Zeko, A.; Sura, S.A.; Turba, R.; Fong, P. Damselfish Stegastes Nigricans Increase Algal Growth within Their Territories on Shallow Coral Reefs via Enhanced Nutrient Supplies. J. Exp. Mar. Biol. Ecol. 2019, 513, 21–26. [Google Scholar] [CrossRef]
- Roach, T.N.F.; Little, M.; Arts, M.G.I.; Huckeba, J.; Haas, A.F.; George, E.E.; Quinn, R.A.; Cobián-Güemes, A.G.; Naliboff, D.S.; Silveira, C.B.; et al. A Multiomic Analysis of in Situ Coral–Turf Algal Interactions. Proc. Natl. Acad. Sci. USA 2020, 117, 13588–13595. [Google Scholar] [CrossRef]
- Ezzat, L.; Merolla, S.; Clements, C.S.; Munsterman, K.S.; Landfield, K.; Stensrud, C.; Schmeltzer, E.R.; Burkepile, D.E.; Vega Thurber, R. Thermal Stress Interacts With Surgeonfish Feces to Increase Coral Susceptibility to Dysbiosis and Reduce Tissue Regeneration. Front. Microbiol. 2021, 12, 620458. [Google Scholar] [CrossRef]
- Ezzat, L.; Lamy, T.; Maher, R.L.; Munsterman, K.S.; Landfield, K.M.; Schmeltzer, E.R.; Clements, C.S.; Vega Thurber, R.L.; Burkepile, D.E. Parrotfish Predation Drives Distinct Microbial Communities in Reef-Building Corals. Anim. Microbiome 2020, 2, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shaver, E.; Shantz, A.; McMinds, R.; Burkepile, D.; Vega Thurber, R.; Silliman, B. Effects of Predation and Nutrient Enrichment on the Success and Microbiome of a Foundational Coral. Ecology 2016, 98, 830–839. [Google Scholar] [CrossRef] [PubMed]
- Zaneveld, J.R.; Burkepile, D.E.; Shantz, A.A.; Pritchard, C.E.; McMinds, R.; Payet, J.P.; Welsh, R.; Correa, A.M.S.; Lemoine, N.P.; Rosales, S.; et al. Overfishing and Nutrient Pollution Interact with Temperature to Disrupt Coral Reefs down to Microbial Scales. Nat. Commun. 2016, 7, 11833. [Google Scholar] [CrossRef]
- Pearse, V.B.; Muscatine, L. Role of Symbiotic Algae (Zooxanthellae) in Coral Calcification. Biol. Bull. 1971, 141, 350–363. [Google Scholar] [CrossRef]
- Rinkevich, B.; Loya, Y. Oriented Translocation of Energy in Grafted Reef Corals. Coral Reefs 1983, 1, 243–247. [Google Scholar] [CrossRef]
- Rinkevich, B.; Loya, Y. Coral Illumination through an Optic Glass-Fiber: Incorporation of 14C Photosynthates. Mar. Biol. 1984, 80, 7–15. [Google Scholar] [CrossRef]
- Hayes, R.L.; Bush, P.G. Microscopic Observations of Recovery in the Reef-Building Scleractinian Coral, Montastrea Annularis, after Bleaching on a Cayman Reef. Coral Reefs 1990, 8, 203–209. [Google Scholar] [CrossRef]
- Hughes, T.P.; Baird, A.H.; Bellwood, D.R.; Card, M.; Connolly, S.R.; Folke, C.; Grosberg, R.; Hoegh-Guldberg, O.; Jackson, J.B.C.; Kleypas, J.; et al. Climate Change, Human Impacts, and the Resilience of Coral Reefs. Science 2003, 301, 929–933. [Google Scholar] [CrossRef] [Green Version]
- D’Angelo, C.; Wiedenmann, J. Impacts of Nutrient Enrichment on Coral Reefs: New Perspectives and Implications for Coastal Management and Reef Survival. Curr. Opin. Environ. Sustain. 2014, 7, 82–93. [Google Scholar] [CrossRef] [Green Version]
- Wooldridge, S. A New Conceptual Model for the Warm-Water Breakdown of the Coral-Algae Endosymbiosis. Mar. Freshw. Res. 2009, 60, 483–496. [Google Scholar] [CrossRef]
- Wooldridge, S.A.; Done, T.J. Improved Water Quality Can Ameliorate Effects of Climate Change on Corals. Ecol. Appl. 2009, 19, 1492–1499. [Google Scholar] [CrossRef] [PubMed]
- Ritchie, K.B. Regulation of Microbial Populations by Coral Surface Mucus and Mucus-Associated Bacteria. Mar. Ecol. Prog. Ser. 2006, 322, 1–14. [Google Scholar] [CrossRef]
- 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. 2007, 9, 2707–2719. [Google Scholar] [CrossRef] [PubMed]
- Robbins, S.J.; Singleton, C.M.; Chan, C.X.; Messer, L.F.; Geers, A.U.; Ying, H.; Baker, A.; Bell, S.C.; Morrow, K.M.; Ragan, M.A.; et al. A Genomic View of the Reef-Building Coral Porites Lutea and Its Microbial Symbionts. Nat. Microbiol. 2019, 4, 2090–2100. [Google Scholar] [CrossRef]
- Rice, M.M.; Maher, R.L.; Vega Thurber, R.; Burkepile, D.E. Different Nitrogen Sources Speed Recovery from Corallivory and Uniquely Alter the Microbiome of a Reef-Building Coral. PeerJ 2019, 7, e8056. [Google Scholar] [CrossRef] [PubMed]
- Zaneveld, J.R.; McMinds, R.; Vega Thurber, R. Stress and Stability: Applying the Anna Karenina Principle to Animal Microbiomes. Nat. Microbiol. 2017, 2, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Shantz, A.A.; Payet, J.P.; Sharpton, T.J.; Foster, A.; Burkepile, D.E.; Vega Thurber, R. Corals and Their Microbiomes Are Differentially Affected by Exposure to Elevated Nutrients and a Natural Thermal Anomaly. Front. Mar. Sci. 2018, 5, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Maher, R.L.; Rice, M.M.; McMinds, R.; Burkepile, D.E.; Vega Thurber, R. Multiple Stressors Interact Primarily through Antagonism to Drive Changes in the Coral Microbiome. Sci. Rep. 2019, 9, 6834. [Google Scholar] [CrossRef] [Green Version]
- Szmant, A. Nutrient Enrichment on Coral Reefs: Is It a Major Cause of Coral Reef Decline? Estuaries 2002, 25, 743–766. [Google Scholar] [CrossRef]
- Fabricius, K. Factors Determining the Resilience of Coral Reefs to Eutrophication: A Review and Conceptual Model. In Coral Reefs: An Ecosystem in Transition; Springer: Dordrecht, The Netherlands, 2011; pp. 493–505. [Google Scholar]
- Thurber, R.L.V.; Burkepile, D.E.; Fuchs, C.; Shantz, A.A.; McMinds, R.; Zaneveld, J.R. Chronic Nutrient Enrichment Increases Prevalence and Severity of Coral Disease and Bleaching. Glob. Chang. Biol. 2014, 20, 544–554. [Google Scholar] [CrossRef]
- 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. 2017, 4, 262. [Google Scholar] [CrossRef] [Green Version]
- Ghanbari, M.; Kneifel, W.; Domig, K.J. A New View of the Fish Gut Microbiome: Advances from next-Generation Sequencing. Aquaculture 2015, 448, 464–475. [Google Scholar] [CrossRef]
- Parris, D.J.; Brooker, R.M.; Morgan, M.A.; Dixson, D.L.; Stewart, F.J. Whole Gut Microbiome Composition of Damselfish and Cardinalfish before and after Reef Settlement. PeerJ 2016, 4, e2412. [Google Scholar] [CrossRef] [Green Version]
- Hester, E.R.; Barott, K.L.; Nulton, J.; Vermeij, M.J.; Rohwer, F.L. Stable and Sporadic Symbiotic Communities of Coral and Algal Holobionts. ISME J. 2016, 10, 1157–1169. [Google Scholar] [CrossRef] [Green Version]
- Parada, A.E.; Needham, D.M.; Fuhrman, J.A. Every Base Matters: Assessing Small Subunit RRNA Primers for Marine Microbiomes with Mock Communities, Time Series and Global Field Samples. Environ. Microbiol. 2016, 18, 1403–1414. [Google Scholar] [CrossRef]
- Apprill, A.; McNally, S.; Parsons, R.; Weber, L. Minor Revision to V4 Region SSU RRNA 806R Gene Primer Greatly Increases Detection of SAR11 Bacterioplankton. Aquat. Microb. Ecol. 2015, 75, 129–137. [Google Scholar] [CrossRef] [Green Version]
- Maher, R.L.; Schmeltzer, E.R.; Meiling, S.; McMinds, R.; Ezzat, L.; Shantz, A.A.; Adam, T.C.; Schmitt, R.J.; Holbrook, S.J.; Burkepile, D.E.; et al. Coral Microbiomes Demonstrate Flexibility and Resilience Through a Reduction in Community Diversity Following a Thermal Stress Event. Front. Ecol. Evol. 2020, 8, 356. [Google Scholar] [CrossRef]
- Callahan, B.J.; McMurdie, P.J.; Rosen, M.J.; Han, A.W.; Johnson, A.J.A.; Holmes, S.P. DADA2: High-Resolution Sample Inference from Illumina Amplicon Data. Nat. Methods 2016, 13, 581–583. [Google Scholar] [CrossRef] [Green Version]
- R: The R Project for Statistical Computing. Available online: https://www.r-project.org/ (accessed on 5 August 2021).
- Quast, C.; Pruesse, E.; Yilmaz, P.; Gerken, J.; Schweer, T.; Yarza, P.; Peplies, J.; Glöckner, F.O. The SILVA Ribosomal RNA Gene Database Project: Improved Data Processing and Web-Based Tools. Nucleic Acids Res. 2013, 41, D590–D596. [Google Scholar] [CrossRef]
- McMurdie, P.J.; Holmes, S. Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE 2013, 8, e61217. [Google Scholar] [CrossRef] [Green Version]
- Bolyen, E.; Rideout, J.R.; Dillon, M.R.; Bokulich, N.A.; Abnet, C.C.; Al-Ghalith, G.A.; Alexander, H.; Alm, E.J.; Arumugam, M.; Asnicar, F.; et al. Author Correction: Reproducible, Interactive, Scalable and Extensible Microbiome Data Science Using QIIME 2. Nat. Biotechnol. 2019, 37, 1091. [Google Scholar] [CrossRef] [PubMed]
- Katoh, K.; Misawa, K.; Kuma, K.; Miyata, T. MAFFT: A Novel Method for Rapid Multiple Sequence Alignment Based on Fast Fourier Transform. Nucleic Acids Res. 2002, 30, 3059–3066. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Price, M.N.; Dehal, P.S.; Arkin, A.P. FastTree 2–Approximately Maximum-Likelihood Trees for Large Alignments. PLoS ONE 2010, 5, e9490. [Google Scholar] [CrossRef] [PubMed]
- Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using Lme4. arXiv 2014, arXiv:1406.5823. [Google Scholar]
- Anderson, M.J. A New Method for Non-Parametric Multivariate Analysis of Variance. Austral. Ecol. 2001, 26, 32–46. [Google Scholar] [CrossRef]
- Anderson, M.J. Distance-Based Tests for Homogeneity of Multivariate Dispersions. Biometrics 2006, 62, 245–253. [Google Scholar] [CrossRef] [PubMed]
- Mandal, S.; Van Treuren, W.; White, R.A.; Eggesbø, M.; Knight, R.; Peddada, S.D. Analysis of Composition of Microbiomes: A Novel Method for Studying Microbial Composition. Microb. Ecol. Health Dis. 2015, 26, 27663. [Google Scholar] [CrossRef] [Green Version]
- Benjamini, Y.; Hochberg, Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc. Ser. B 1995, 57, 289–300. [Google Scholar] [CrossRef]
- Leichter, J.; Seydel, K.; Gotschalk, C. MCR LTER: Coral Reef: Benthic Water Temperature, Ongoing Since 2005 Ver 11. Available online: https://doi.org/10.6073/pasta/1a5760c3146c574c98db854ad6d3addc (accessed on 2 April 2021).
- Washburn, L.; Brooks, A.J. MCR LTER: Coral Reef: Gump Station Meteorological Data, Ongoing since 2006 Ver 45. Available online: https://doi.org/10.6073/pasta/70821c6834ad8cef72515ba107618738 (accessed on 2 April 2021).
- Bernhardt, H.; Wilhelms, A. The Continuous Determination of Low Level Iron, Soluble Phosphate and Total Phosphate with the AutoAnalyzer TM. Technicon Symp. 1967, 1, 386. [Google Scholar]
- Armstrong, F.A.J.; Stearns, C.R.; Strickland, J.D.H. The Measurement of Upwelling and Subsequent Biological Process by Means of the Technicon Autoanalyzer® and Associated Equipment. Deep Sea Res. A 1967, 14, 381–389. [Google Scholar] [CrossRef]
- Patton, C.J. Design, Characterization and Applications of a Miniature Continuous Flow Analysis System. Ph.D. Thesis, Michigan State University, East Lansing, MI, USA, 1983. [Google Scholar]
- Gordon, L.; Jennings, J.; Ross, A.; Krest, J. A Suggested Protocol for Continuous Flow Automated Analysis of Seawater Nutrients (Phosphate, Nitrate, Nitrite and Silicic Acid) in the WOCE Hydrographic Program and the Joint Global Ocean Fluxes Study. 1993, p. 91. Available online: http://www.ioccp.org/images/06Nutrients/WOCE_nutrients-manual_1993.pdf (accessed on 2 August 2021).
- Vega Thurber, R.; Willner-Hall, D.; Rodriguez-Mueller, B.; Desnues, C.; Edwards, R.A.; Angly, F.; Dinsdale, E.; Kelly, L.; Rohwer, F. Metagenomic Analysis of Stressed Coral Holobionts. Environ. Microbiol. 2009, 11, 2148–2163. [Google Scholar] [CrossRef]
- Neave, M.J.; Apprill, A.; Ferrier-Pagès, C.; Voolstra, C.R. Diversity and Function of Prevalent Symbiotic Marine Bacteria in the Genus Endozoicomonas. Appl. Microbiol. Biotechnol. 2016, 100, 8315–8324. [Google Scholar] [CrossRef] [Green Version]
- Shade, A.; Peter, H.; Allison, S.D.; Baho, D.; Berga, M.; Buergmann, H.; Huber, D.H.; Langenheder, S.; Lennon, J.T.; Martiny, J.B.; et al. Fundamentals of Microbial Community Resistance and Resilience. Front. Microbiol. 2012, 3, 417. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Griffiths, B.S.; Ritz, K.; Bardgett, R.D.; Cook, R.; Christensen, S.; Ekelund, F.; Sørensen, S.J.; Bååth, E.; Bloem, J.; Ruiter, P.C.D.; et al. Ecosystem Response of Pasture Soil Communities to Fumigation-Induced Microbial Diversity Reductions: An Examination of the Biodiversity–Ecosystem Function Relationship. Oikos 2000, 90, 279–294. [Google Scholar] [CrossRef]
- Wittebolle, L.; Marzorati, M.; Clement, L.; Balloi, A.; Daffonchio, D.; Heylen, K.; De Vos, P.; Verstraete, W.; Boon, N. Initial Community Evenness Favours Functionality under Selective Stress. Nature 2009, 458, 623–626. [Google Scholar] [CrossRef]
- Ceccarelli, D.M.; Jones, G.P.; McCook, L.J. Territorial Damselfishes as Determinants of the Structure of Benthic Communities on Coral Reefs. Oceanogr. Mar. Biol. Annu. Rev. 2001, 39, 355–389. [Google Scholar]
- Meekan, M.G.; Steven, A.D.L.; Fortin, M.J. Spatial Patterns in the Distribution of Damselfishes on a Fringing Coral Reef. Coral Reefs 1995, 14, 151–161. [Google Scholar] [CrossRef]
- Bender-Champ, D.; Diaz-Pulido, G.; Dove, S. Effects of Elevated Nutrients and CO2 Emission Scenarios on Three Coral Reef Macroalgae. Harmful Algae 2017, 65, 40–51. [Google Scholar] [CrossRef] [PubMed]
- Gibbin, E.; Gavish, A.; Krueger, T.; Kramarsky-Winter, E.; Shapiro, O.; Guiet, R.; Jensen, L.; Vardi, A.; Meibom, A. Vibrio Coralliilyticus Infection Triggers a Behavioural Response and Perturbs Nutritional Exchange and Tissue Integrity in a Symbiotic Coral. ISME J. 2019, 13, 989–1003. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pollock, F.J.; Morris, P.J.; Willis, B.L.; Bourne, D.G. Detection and Quantification of the Coral Pathogen Vibrio Coralliilyticus by Real-Time PCR with TaqMan Fluorescent Probes. Appl. Environ. Microbiol. 2010, 76, 5282–5286. [Google Scholar] [CrossRef] [Green Version]
- Sussman, M.; Mieog, J.C.; Doyle, J.; Victor, S.; Willis, B.L.; Bourne, D.G. Vibrio Zinc-Metalloprotease Causes Photoinactivation of Coral Endosymbionts and Coral Tissue Lesions. PLoS ONE 2009, 4, e4511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de O Santos, E.; Alves, N.; Dias, G.M.; Mazotto, A.M.; Vermelho, A.; Vora, G.J.; Wilson, B.; Beltran, V.H.; Bourne, D.G.; Le Roux, F.; et al. Genomic and Proteomic Analyses of the Coral Pathogen Vibrio Coralliilyticus Reveal a Diverse Virulence Repertoire. ISME J. 2011, 5, 1471–1483. [Google Scholar] [CrossRef] [PubMed]
- Luo, D.; Wang, X.; Feng, X.; Tian, M.; Wang, S.; Tang, S.-L.; Ang, P.; Yan, A.; Luo, H. Population Differentiation of Rhodobacteraceae along with Coral Compartments. ISME J. 2021, 15, 1–17. [Google Scholar] [CrossRef]
- Fabricius, K.E. Effects of Terrestrial Runoff on the Ecology of Corals and Coral Reefs: Review and Synthesis. Mar. Pollut. Bull. 2005, 50, 125–146. [Google Scholar] [CrossRef] [PubMed]
- Stambler, N.; Popper, N.; Dubinsky, Z.; Stimson, J. Effects of Nutrient Enrichment and Water Motion on the Coral Pocillopora Damicornis. 1991. Available online: https://scholarspace.manoa.hawaii.edu/bitstream/10125/1396/v45n3-299-307.pdf (accessed on 6 June 2021).
- Dougan, K.E.; Ladd, M.C.; Fuchs, C.; Vega Thurber, R.; Burkepile, D.E.; Rodriguez-Lanetty, M. Nutrient Pollution and Predation Differentially Affect Innate Immune Pathways in the Coral Porites Porites. Front. Mar. Sci. 2020, 7, 742–751. [Google Scholar] [CrossRef]
- Morris, L.A.; Voolstra, C.R.; Quigley, K.M.; Bourne, D.G.; Bay, L.K. Nutrient Availability and Metabolism Affect the Stability of Coral–Symbiodiniaceae Symbioses. Trends Microbiol. 2019, 27, 678–689. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Messyasz, A.; Maher, R.L.; Meiling, S.S.; Thurber, R.V. Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals. Microorganisms 2021, 9, 1873. https://doi.org/10.3390/microorganisms9091873
Messyasz A, Maher RL, Meiling SS, Thurber RV. Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals. Microorganisms. 2021; 9(9):1873. https://doi.org/10.3390/microorganisms9091873
Chicago/Turabian StyleMessyasz, Adriana, Rebecca L. Maher, Sonora S. Meiling, and Rebecca Vega Thurber. 2021. "Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals" Microorganisms 9, no. 9: 1873. https://doi.org/10.3390/microorganisms9091873
APA StyleMessyasz, A., Maher, R. L., Meiling, S. S., & Thurber, R. V. (2021). Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals. Microorganisms, 9(9), 1873. https://doi.org/10.3390/microorganisms9091873