Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals

Adriana Messyasz,Rebecca Vega Thurber,Rebecca L Maher,Sonora S Meiling

doi:10.3390/microorganisms9091873

Abstract

While studies show that nutrient pollution shifts reef trophic interactions between fish, macroalgae, and corals, we know less about how the microbiomes associated with these organisms react to such disturbances. To investigate how microbiome dynamics are affected during nutrient pollution, we exposed replicate Porites lobata corals colonized by the fish Stegastes nigricans, which farm an algal matrix on the coral, to a pulse of nutrient enrichment over a two-month period and examined the microbiome of each partner using 16S amplicon analysis. We found 51 amplicon sequence variants (ASVs) shared among the three hosts. Coral microbiomes had the lowest diversity with over 98% of the microbiome dominated by a single genus, Endozoicomonas. Fish and algal matrix microbiomes were ~20 to 70× more diverse and had higher evenness compared to the corals. The addition of nutrients significantly increased species richness and community variability between samples of coral microbiomes but not the fish or algal matrix microbiomes, demonstrating that coral microbiomes are less resistant to nutrient pollution than their trophic partners. Furthermore, the 51 common ASVs within the 3 hosts indicate microbes that may be shared or transmitted between these closely associated organisms, including Vibrionaceae bacteria, many of which can be pathogenic to corals.

Highlights

Porites lobata colonies inhabited by Stegastes nigricans fish that were actively farming turf algae were used for this experiment
Given this link to nutrient enrichment and increased disease and mortality from fish predation, we posited that symbioses between algal matrix farming fishes and their coral hosts would be negatively affected by the addition of nitrogen and phosphorus into highly oligotrophic habitats such as those on the island of Mo’orea
Our study is first to examine the microbiomes of three closely-associated hosts in the coral reef ecosystem under one experimental nutrient-pulse period

Summary

Introduction

It is well established that nutrient enrichment can increase macroalgal growth in the absence of fish herbivory, resulting in corals becoming overgrown, shaded, and/or diseased [2,3,4,5]. These combined negative effects on coral physiological traits (inhibition of coral recruitment and growth) can shift a reef from a coral-dominated to algal-dominated state which makes corals less resilient to disturbances such as bleaching, disease, and hurricanes [5,6,7,8,9].

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Discussion

Conclusion