Dataset Information

Microbiome Dynamics in a Large Artificial Seawater Aquarium.

ABSTRACT: Artificial habitats for animals have high commercial and societal value. Microbial communities (microbiomes) in such habitats may play ecological roles similar to those in nature. However, this hypothesis remains largely untested. Georgia Aquarium's Ocean Voyager (OV) exhibit is a closed-system aquatic habitat that mimics the oligotrophic open ocean and houses thousands of large marine animals, including fish, sea turtles, and whale sharks. We present a 14-month time series characterizing the OV water column microbiome. The composition and stability of the microbiome differed from those of natural marine environments with similar chemical features. The composition shifted dramatically over the span of 2 weeks and was characterized by bloom events featuring members of two heterotrophic bacterial lineages with cosmopolitan distributions in the oceans. The relative abundances of these lineages were inversely correlated, suggesting an overlap in ecological niches. Transcript mapping to metagenome-assembled genomes (MAGs) of these taxa identified unique characteristics, including the presence and activity of genes for the synthesis and degradation of cyanophycin, an amino acid polymer linked to environmental stress and found frequently in cyanobacteria but rarely in heterotrophic bacteria. The dominant MAGs also contained and transcribed plasmid-associated sequences, suggesting a role for conjugation in adaptation to the OV environment. These findings indicate a highly dynamic microbiome despite the stability of the physical and chemical parameters of the water column. Characterizing how such fluctuations affect microbial function may inform our understanding of animal health in closed aquaculture systems.IMPORTANCE Public aquariums play important societal roles, for example, by promoting science education and helping conserve biodiversity. The health of aquarium animals depends on interactions with the surrounding microbiome. However, the extent to which aquariums recreate a stable and natural microbial ecosystem is uncertain. This study describes the taxonomic composition of the water column microbiome over 14 months in a large indoor aquatic habitat, the Ocean Voyager exhibit at the Georgia Aquarium. Despite stable water column conditions, the exhibit experienced blooms in which the abundance of a single bacterial strain increased to over 65% of the community. Genome analysis indicated that the OV's dominant strains share unique adaptations, notably genes for storage polymers associated with environmental stress. These results, interpreted alongside data from natural ocean systems and another artificial seawater aquarium, suggest a highly dynamic aquarium microbiome and raise questions of how microbiome stability may affect the ecological health of the habitat.

SUBMITTER: Patin NV

PROVIDER: S-EPMC5930379 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Microbiome Dynamics in a Large Artificial Seawater Aquarium.

Patin Nastassia V NV Pratte Zoe A ZA Regensburger Matthew M Hall Eric E Gilde Kailen K Dove Alistair D M ADM Stewart Frank J FJ

Applied and environmental microbiology 20180501 10

Artificial habitats for animals have high commercial and societal value. Microbial communities (microbiomes) in such habitats may play ecological roles similar to those in nature. However, this hypothesis remains largely untested. Georgia Aquarium's <i>Ocean Voyager</i> (OV) exhibit is a closed-system aquatic habitat that mimics the oligotrophic open ocean and houses thousands of large marine animals, including fish, sea turtles, and whale sharks. We present a 14-month time series characterizing ...[more]

PMID: 29523545

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Project description:BackgroundAnimal-associated microbiomes can be influenced by both host and environmental factors. Comparing wild animals to those in zoos or aquariums can help disentangle the effects of host versus environmental factors, while also testing whether managed conditions foster a 'natural' host microbiome. Focusing on an endangered elasmobranch species-the whitespotted eagle ray Aetobatus narinari-we compared the skin, gill, and cloaca microbiomes of wild individuals to those at Georgia Aquarium. Whitespotted eagle ray microbiomes from Georgia Aquarium were also compared to those of cownose rays (Rhinoptera bonasus) in the same exhibit, allowing us to explore the effect of host identity on the ray microbiome.ResultsLong-term veterinary monitoring indicated that the rays in managed care did not have a history of disease and maintained health parameters consistent with those of wild individuals, with one exception. Aquarium whitespotted eagle rays were regularly treated to control parasite loads, but the effects on animal health were subclinical. Microbiome α- and β-diversity differed between wild versus aquarium whitespotted eagle rays at all body sites, with α-diversity significantly higher in wild individuals. β-diversity differences in wild versus aquarium whitespotted eagle rays were greater for skin and gill microbiomes compared to those of the cloaca. At each body site, we also detected microbial taxa shared between wild and aquarium eagle rays. Additionally, the cloaca, skin, and gill microbiomes of aquarium eagle rays differed from those of cownose rays in the same exhibit. Potentially pathogenic bacteria were at low abundance in all wild and aquarium rays.ConclusionFor whitespotted eagle rays, managed care was associated with a microbiome differing significantly from that of wild individuals. These differences were not absolute, as the microbiome of aquarium rays shared members with that of wild counterparts and was distinct from that of a cohabitating ray species. Eagle rays under managed care appear healthy, suggesting that their microbiomes are not associated with compromised host health. However, the ray microbiome is dynamic, differing with both environmental factors and host identity. Monitoring of aquarium ray microbiomes over time may identify taxonomic patterns that co-vary with host health.

Project description:Denitrification by sulfur-oxidizing bacteria is an effective nitrate removal strategy in engineered aquatic systems. However, the community taxonomic and metabolic diversity of sulfur-driven denitrification (SDN) systems, as well as the relationship between nitrate removal and SDN community structure, remains underexplored. This is particularly true for SDN reactors applied to marine aquaria, despite the increasing use of this technology to supplement filtration. We applied 16S rRNA gene, metagenomic, and metatranscriptomic analyses to explore the microbial basis of SDN reactors operating on Georgia Aquarium's Ocean Voyager, the largest indoor closed-system seawater exhibit in the United States. The exhibit's two SDN systems vary in water retention time and nitrate removal efficiency. The systems also support significantly different microbial communities. These communities contain canonical SDN bacteria, including a strain related to Thiobacillus thioparus that dominates the system with the higher water retention time and nitrate removal but is effectively absent from the other system. Both systems contain a wide diversity of other microbes whose metagenome-assembled genomes contain genes of SDN metabolism. These include hundreds of strains of the epsilonproteobacterium Sulfurimonas, as well as gammaproteobacterial sulfur oxidizers of the Thiotrichales and Chromatiales, and a relative of Sedimenticola thiotaurini with complete denitrification potential. The SDN genes are transcribed and the taxonomic richness of the transcript pool varies markedly among the enzymatic steps, with some steps dominated by transcripts from noncanonical SDN taxa. These results indicate complex and variable SDN communities that may involve chemical dependencies among taxa as well as the potential for altering community structure to optimize nitrate removal.IMPORTANCE Engineered aquatic systems such as aquaria and aquaculture facilities have large societal value. Ensuring the health of animals in these systems requires understanding how microorganisms contribute to chemical cycling and waste removal. Focusing on the largest seawater aquarium in the United States, we explore the microbial communities in specialized reactors designed to remove excess nitrogen through the metabolic activity of sulfur-consuming microbes. We show that the diversity of microbes in these reactors is both high and highly variable, with distinct community types associated with significant differences in nitrogen removal rate. We also show that the genes encoding the metabolic steps of nitrogen removal are distributed broadly throughout community members, suggesting that the chemical transformations in this system are likely a result of microbes relying on other microbes. These results provide a framework for future studies exploring the contributions of different community members, both in waste removal and in structuring microbial biodiversity.

Dataset Information

Microbiome Dynamics in a Large Artificial Seawater Aquarium.

Publications

Microbiome Dynamics in a Large Artificial Seawater Aquarium.

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