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Research Article | Applied and Environmental Science

Component Microenvironments and System Biogeography Structure Microorganism Distributions in Recirculating Aquaculture and Aquaponic Systems

Ryan P. Bartelme, Matthew C. Smith, Osvaldo J. Sepulveda-Villet, Ryan J. Newton
Hideyuki Tamaki, Editor
Ryan P. Bartelme
aSchool of Freshwater Sciences, University of Wisconsin—Milwaukee, Milwaukee, Wisconsin, USA
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  • ORCID record for Ryan P. Bartelme
Matthew C. Smith
aSchool of Freshwater Sciences, University of Wisconsin—Milwaukee, Milwaukee, Wisconsin, USA
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Osvaldo J. Sepulveda-Villet
aSchool of Freshwater Sciences, University of Wisconsin—Milwaukee, Milwaukee, Wisconsin, USA
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Ryan J. Newton
aSchool of Freshwater Sciences, University of Wisconsin—Milwaukee, Milwaukee, Wisconsin, USA
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Hideyuki Tamaki
National Institute of Advanced Industrial Science and Technology
Roles: Editor
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DOI: 10.1128/mSphere.00143-19
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Figures

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  • FIG 1
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    FIG 1

    Dendrogram of bacterial community dissimilarity across University of Wisconsin–Milwaukee RAS components. The dendrogram was created using average-linkage Bray-Curtis dissimilarity of bacterial communities between RAS components. Leaves are labeled by date and sample site within the RAS. Sample site references are as follows, in order of process flow: Tank, rearing tank; pH, pH buffering tank; Clar, clarifier sludge; ClarOut, clarifier effluent; Bfsand, biofilter sand substrate, BfOut, biofilter effluent; Degas, carbon dioxide degassing tower.

  • FIG 2
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    FIG 2

    Nonmetric multidimensional scaling (nMDS) plot of bacterial community composition. The plot indicates Bray-Curtis dissimilarity between samples (V4-V5 16S rRNA gene data) as ordinated by the metaMDS function with dimensions k = 5 and stress = 0.078. Data in ellipses are illustrated as follows: (A) all samples from a particular site (ADONIS R2 = 0.355, P ≤ 0.001) and (B) all samples from a particular water source (ADONIS R2 = 0.110, P ≤ 0.001). Ellipses were added with the ordiellipse function in vegan (70). The component origin of each sample is indicated via the shape of the sample point as indicated in the figure key. UWM, University of Wisconsin—Milwaukee.

  • FIG 3
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    FIG 3

    Heat map of the most abundant 16S rRNA gene amplicon sequence variants across component types. The plot indicates bacterial community composition relative to abundance data ordered by distance-based clustering (Euclidian) of samples containing only the illustrated amplicon sequence variants (ASVs). The top 10 most abundant ASVs (mean relative abundances) for each major component type, biofilter, solids, and rearing tank are plotted (heatmap2 from the ggplots R package). The ASVs are also ordered by distance-based clustering (Euclidian) of their relative abundance patterns. Gene relative abundances are indicated via color-coding as listed in the plot key. Each sample’s component type and sample site origin are indicated below the heat map. The sample name abbreviations are as follows: Bell, Bell Aquaculture; DW, Discovery World; PF, PortFish; UFP, UrbanFarmProject; MAR, Marinette. Family-level and genus-level taxonomic assignments are listed for each ASV. When these levels were not assigned, then the most refined taxonomic level is provided. Identical taxonomic assignments are given a number (indicated in square brackets) to facilitate references in the text. na, unassigned taxonomy at this level.

  • FIG 4
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    FIG 4

    Presence/absence heat map of nitrifying microorganism amplicon sequence variants (ASVs). Samples are included as rows, and sample facilities are indicated. Columns represent unique ASVs (>95% nucleotide sequence identity) ordered by taxonomic affiliation as indicated. The presence of an ASV in a sample is indicated by a colored square. ASV designations are indicated along the x axis. Sequence alignments and phylogenies for Betaproteobacteria amoA, Nitrospira nxrB, and Nitrospira amoA ASVs can be found at https://doi.org/10.6084/m9.figshare.7777232.v1, https://doi.org/10.6084/m9.figshare.7777241.v2, and https://doi.org/10.6084/m9.figshare.7777247.v1.

  • FIG 5
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    FIG 5

    Richness distribution for recovered nxrB genotypes between RAS and aquaponic samples. Pirate plots (“yarrr” package in R) are indicated for nxrB genotype richness for each sample class (aquaponic or RAS). A black line indicates the richness mean, a colored box indicates the Bayesian highest-density interval, and all points are listed with corresponding indication of data distribution/density via figure shape.

  • FIG 6
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    FIG 6

    Generalized component process diagram. Black arrows indicate the flow of the water through the University of Wisconsin—Milwaukee (UWM) system. The dashed green arrows represent the generalized flow of water in the aquaponic systems.

Tables

  • Figures
  • Supplemental Material
  • TABLE 1

    Alpha-diversity metrics across UWM RAS sites

    SiteaH' ± SDbJ ± SDcndSample
    categorye
    Biofilter effluent4.22 ± 0.320.68 ± 0.054Plankton
    Biofilter sand4.66 ± 0.200.75 ± 0.046Biofilm
    Biofilter water4.26 ± 0.740.68 ± 0.124Plankton
    Clarifier4.27 ± 0.210.68 ± 0.036Sludge
    Clarifier effluent4.38 ± 0.350.70 ± 0.064Plankton
    Degasser4.20 ± 0.310.67 ± 0.055Plankton
    pH buffer tank3.54 ± 1.410.57 ± 0.223Plankton
    Rearing tank4.13 ± 0.130.66 ± 0.024Plankton
    • ↵a All alpha-diversity metrics were calculated across the University of Wisconsin—Milwaukee Recirculating Aquaculture System sites using the V6 16S rRNA gene sequence data set.

    • ↵b Data represent Shannon-Weaver diversity index (H’) values. Standard deviation (SD) values are indicated after the mean values.

    • ↵c Data represent Pielou’s evenness metric (J) values. Standard deviation (SD) values are indicated after the mean values.

    • ↵d The number of samples at each site is indicated.

    • ↵e Sample categories used in Kruskall-Wallis rank sum hypothesis testing are indicated.

  • TABLE 2

    PCR primers used in this study

    Gene targetForward primer(s)
    (5′–3′)
    Reverse primer(s)
    (5′–3′)
    Component(s)
    surveyed
    Sample
    site(s)
    Reference(s)
    Bacterial 16S rRNA gene
    V6 region
    CTAACCGANGAACCTYACC,
    CNACGCGAAGAACCTTANC,
    CAACGCGMARAACCTTACC,
    ATACGCGARGAACCTTACC
    CGACRRCCATGCANCACCTAllUWM RAS72
    Bacterial 16S rRNA gene
    V4-V5 region
    CCAGCAGCYGCGGTAANCCGTCAATTCNTTTRAGT,
    CCGTCAATTTCTTTGAGT,
    CCGTCTATTCCTTTGANT
    AllAll73
    Archaeal 16S rRNA gene
    V4-V5 region
    GCCTAAAGCATCCGTAGC,
    GCCTAAARCGTYCGTAGC,
    GTCTAAAGGGTCYGTAGC,
    GCTTAAAGNGTYCGTAGC,
    GTCTAAARCGYYCGTAGC
    CCGGCGTTGANTCCAATTBiofiltersAll biofilter samples74
    Betaproteobacterial amoAGGGGHTTYTACTGGTGGTCCCCTCKGSAAAGCCTTCTTCBiofiltersAll Biofilter Samples75, 76
    Comammox amoAGGAYTTYTGGNTNGATTGGAWRKTNNGACCACCASKACCABiofiltersAll biofilter samplesModified from
    reference 58
    Nitrospira nxrBTACATGTGGTGGAACACGGTTCTGGTCRATCABiofiltersAll biofilter samples53

Supplemental Material

  • Figures
  • Tables
  • TABLE S1

    Sample list and associated metadata for the V6 and V4-V5 16S rRNA gene sequence datasets. Download Table S1, XLSX file, 0.1 MB.

    Copyright © 2019 Bartelme et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Component Microenvironments and System Biogeography Structure Microorganism Distributions in Recirculating Aquaculture and Aquaponic Systems
Ryan P. Bartelme, Matthew C. Smith, Osvaldo J. Sepulveda-Villet, Ryan J. Newton
mSphere Jul 2019, 4 (4) e00143-19; DOI: 10.1128/mSphere.00143-19

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Component Microenvironments and System Biogeography Structure Microorganism Distributions in Recirculating Aquaculture and Aquaponic Systems
Ryan P. Bartelme, Matthew C. Smith, Osvaldo J. Sepulveda-Villet, Ryan J. Newton
mSphere Jul 2019, 4 (4) e00143-19; DOI: 10.1128/mSphere.00143-19
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    • ABSTRACT
    • INTRODUCTION
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KEYWORDS

Flavobacterium
Nitrospira
ammonia-oxidizing Archaea
aquaponics
biofilter
comammox
microbial community composition
nitrifiers
recirculating aquaculture system

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