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Research Article | Ecological and Evolutionary Science

Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems

Sara F. Paver, Daniel Muratore, Ryan J. Newton, Maureen L. Coleman
Theodore M. Flynn, Editor
Sara F. Paver
aDepartment of the Geophysical Sciences, University of Chicago, Chicago, Illinois, USA
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Daniel Muratore
aDepartment of the Geophysical Sciences, University of Chicago, Chicago, Illinois, USA
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Ryan J. Newton
bSchool of Freshwater Sciences, University of Wisconsin Milwaukee, Milwaukee, Wisconsin, USA
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Maureen L. Coleman
aDepartment of the Geophysical Sciences, University of Chicago, Chicago, Illinois, USA
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Theodore M. Flynn
Argonne National Laboratory
Roles: Editor
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DOI: 10.1128/mSystems.00232-18
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  • FIG 1
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    FIG 1

    Median relative abundance of phyla/proteobacterial classes in freshwater and marine samples collected from surface (a) and deep (b) waters. The deepest hypolimnion (below thermocline) sample collected from stratified lakes and marine samples collected at depths >75m were classified as “deep” samples. Diagonal lines indicate a 1:1 relationship.

  • FIG 2
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    FIG 2

    Species accumulation curves for taxonomic groups that contain shared marine and freshwater MED nodes as the number of freshwater sites included in the analysis increases (a) and as the number of marine sites included in the analysis increases (b). The percentage of sequences shared between habitats with all sites analyzed is included to the right of each curve; the total number of MED nodes within each group in freshwater and marine habitats, respectively, is indicated in parentheses.

  • FIG 3
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    FIG 3

    Maximum sequence identity threshold (i.e., finest-scale resolution) at which pairs of marine and freshwater samples share common taxa. Box plots indicate the median, quartiles, and range of values observed for all marine-freshwater sample pairs. Colored boxes indicate phyla/proteobacterial classes that contain 5 or more shared MED nodes while gray boxes indicate groups that contain 1 to 3 shared MED nodes. The heatmap to the right illustrates the number of freshwater (F) and marine (M) samples containing representatives of each phylum/proteobacterial class. *, Actinobacteria cutoff values were calculated with a preclustered data set (see Fig. S5 for comparison of all groups using a preclustered data set).

  • FIG 4
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    FIG 4

    Observations of non-LD12 SAR11. (a) 16S rRNA V4 region gene tree constructed using representative sequences from each SAR11 node. The first ring indicates whether nodes were found only in marine (blue) or freshwater samples (green) while the second ring indicates nodes that are shared across habitat types (orange). (b) Number of non-LD12 SAR11 clade sequences detected at four stations (MI18M, MI27M, MI41M, ON33M) and three depths (SRF, surface; DCL, deep chlorophyll maximum layer; BOT, near-bottom) on Lakes Michigan and Ontario.

  • FIG 5
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    FIG 5

    Metagenomic evidence for non-LD12 SAR11 in the Laurentian Great Lakes. (a) Percentage of classified reads identified as LD12 (green) in an open ocean sample (Marine), compared to marine (i.e., non-LD12) SAR11 (blue) in each of the five Laurentian Great Lakes (SU, Superior; MI, Michigan; HU, Huron; ER, Erie; ON, Ontario). Ridge plots present the distribution of identified reads across all protein clusters with greater than 100 reads classified as SAR11 or LD12 at a likelihood value of 0.95. (b) Neighbor-joining consensus tree of 1.2-kb nucleotide sequences from the protein cluster identified as COG2609 (pyruvate dehydrogenase complex, dehydrogenase E1 component). Strain names are colored based on phylogenetic classification within the SAR11 clade: green, LD12 sequences from group IIIb; light blue, group IIIa, sister group to IIIb; medium blue, all other marine SAR11 clades included in the analysis (Ia, II); black, a contig assembled from the Lake Erie metagenome. Consensus support values (%) are indicated on branches.

Tables

  • Figures
  • Supplemental Material
  • TABLE 1

    Genera containing at least two shared MED nodes

    Phylum/classOrderFamilyGenusbNo. of
    shared
    nodes
    ActinobacteriaAcidimicrobialesOM1_clade“Ca. Actinomarina”2
    ActinobacteriaAcidimicrobialesSva0996aSva0996a2
    ActinobacteriaCorynebacterialesMycobacteriaceaeMycobacterium2
    ActinobacteriaMicrococcalesMicrobacteriaceae“Ca. Aquiluna”4
    ActinobacteriaPeM15PeM15PeM154
    BacteroidetesFlavobacterialesCryomorphaceaeFluviicola5
    BacteroidetesSphingobacterialesChitinophagaceaeSediminibacterium2
    BacteroidetesSphingobacterialesNS11-12aNS11-12a3
    CyanobacteriaSubsection IFamily ISynechococcus3
    MarinimicrobiaSAR406 cladeSAR406 cladeSAR406 clade4
    AlphaproteobacteriaCaulobacteralesCaulobacteraceaeBrevundimonas4
    AlphaproteobacteriaRhizobialesMethylobacteriaceaeMethylobacterium3
    AlphaproteobacteriaSphingomonadalesSphingomonadaceaeNovosphingobium2
    AlphaproteobacteriaSphingomonadalesSphingomonadaceaeSphingobium3
    AlphaproteobacteriaSphingomonadalesSphingomonadaceaeSphingomonas3
    BetaproteobacteriaBurkholderialesBurkholderiaceaeRalstonia2
    BetaproteobacteriaBurkholderialesComamonadaceaeAquabacterium2
    DeltaproteobacteriaSAR324 cladeSAR324 cladeSAR324 clade3
    GammaproteobacteriaAlteromonadalesAlteromonadaceaeMarinobacter2
    GammaproteobacteriaE01-9C-26aE01-9C-26aE01-9C-26a2
    GammaproteobacteriaOceanospirillalesOceanospirillaceaePseudohongiella4
    GammaproteobacteriaOceanospirillalesOM182 cladeOM182 clade2
    GammaproteobacteriaOceanospirillalesSAR86 cladeSAR86 clade2
    GammaproteobacteriaPseudomonadalesMoraxellaceaeAcinetobacter5
    GammaproteobacteriaPseudomonadalesPseudomonadaceaePseudomonas3
    GammaproteobacteriaVibrionalesVibrionaceaeVibrio2
    EuryarchaeotaThermoplasmatalesMarine group IIMarine group II2
    ThaumarchaeotaUnknown orderUnknown family“Ca. Nitrosopumilus”2
    • ↵a Marine group.

    • ↵b Ca., Candidatus.

  • TABLE 2

    16S rRNA v4 region sequencing data sets included in the meta-analysis

    No. of samplesStudy systemDepth(s) sampledaBioProject accession no.
    (reference)
    Freshwater samples (45 total)
        11Four Laurentian Great LakesSurface, DCL, deepThis study
        2Glacier Lake, NY6 m, 14 mPRJEB12903
        1JBL_J07_HES, SwedenIntegratedPRJNA244610 (79)
        1Lake Keluke, ChinaSurfacePRJNA294836 (80)
        1Faselfad lakes, AustriaIntegratedPRJNA297573 (81)
        14Seven high-nutrient lakes, MISurface, deepPRJNA304344 (82)
        9Five low-nutrient lakes, MISurface, deepPRJNA304344 (82)
        6Three humic lakes, WIIntegrated epi, integrated hypoPRJEB15148 (83)
    Marine samples (32 total)
        1Caribbean SeaSurfacePRJEB10633 (28)
        2Coastal Red Sea (2 sites)SurfacePRJNA279146 (54)
        1Drake PassageSurfacePRJEB10633 (28)
        12Gulf of Mexico (3 sites)Surface, multiple depthsPRJNA327040 (84)
        1Helgoland North SeaSurfacePRJNA266669 (85)
        1Long Island SoundSurfacePRJEB10633 (28)
        2North PacificSurface, 100 mPRJEB10633 (28)
        8San Pedro Ocean Time Series (2 dates: April,
    July 2013)
    Surface, multiple depthsPRJEB10633 (28)
        2Sargasso Sea (2 sites)Surface, 200 mPRJEB10633 (28)
        1Tropical Western Atlantic Ocean40 mPRJEB10633 (28)
        1Weddell SeaSurfacePRJEB10633 (28)
    • ↵a Abbreviations: DCL, deep chlorophyll layer; epi, epilimnion; hypo, hypolimnion.

  • TABLE 3

    SAR11 and LD12 genomes included in pangenomic analysis

    Genome nameSAR11 cladeClassificationGenBank accession no.
    Alphaproteobacterium HIMB114IIIaSAR11NZ_ADAC02000001
    Alphaproteobacterium HIMB59VSAR11NC_018644
    “Candidatus Pelagibacter” sp. HTCC7211Ia.2SAR11ABVS00000000
    “Candidatus Pelagibacter” sp. IMCC9063IIIaSAR11NC_015380
    “Candidatus Pelagibacter ubique” HIMB058IISAR11ATTF01000000
    “Candidatus Pelagibacter ubique” HIMB083Ia.2SAR11AZAL00000000
    “Candidatus Pelagibacter ubique” HTCC1062Ia.1SAR11NC_007205
    “Candidatus Pelagibacter ubique” HTCC8051Ia.2SAR11AWZY00000000
    SCGC AAA280-B11IIIbLD12AQUH00000000
    SCGC AAA027-C06IIIbLD12AQPD00000000
    SCGC AAA028-C07IIIbLD12ATTB01000000
    SCGC AAA028-D10IIIbLD12AZOF00000000
    SCGC AAA280-P20IIIbLD12AQUE00000000
    SCGC AAA023-L09IIIbLD12ATTD01000000
    SCGC AAA027-L15IIIbLD12AQUG00000000
    SCGC AAA487-M09IIIbLD12ATTC00000000
    SCGC AAA024-N17IIIbLD12AQZA00000000
    SCGC AAA280-P20IIIbLD12AQUE00000000
    “Candidatus Fonsibacter ubiquis” LSUCC0530IIIbLD12NZ_CP024034
    Lake_Baikal_MAGUnknownSAR11NSIJ01000001

Supplemental Material

  • Figures
  • Tables
  • FIG S1

    Log10 fold change as a function of log10-transformed median relative abundances in each habitat plotted for orders (a, b) and families (c, d) in freshwater (a, c) and marine (b, d) systems. A solid gray line is plotted at a log10 fold change of 0, indicating that marine and freshwater median relative abundances are equal. Dotted gray lines are plotted at log10 fold changes of 1 and −1, which correspond to median abundance in one habitat being 10× higher than the median abundance in the other habitat. Download FIG S1, EPS file, 0.5 MB.

    Copyright © 2018 Paver et al.

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

  • FIG S2

    Principal coordinate analysis of unweighted UniFrac distances between marine and freshwater assemblages characterized by 16S rRNA V4 gene sequences (a). The same ordination color coded by nutrient classification and labeling a group of outlier freshwater samples as those collected from dystrophic bog lakes (b). Download FIG S2, EPS file, 0.5 MB.

    Copyright © 2018 Paver et al.

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

  • FIG S3

    Median unweighted UniFrac distances (bars indicate range) between pairs of freshwater and marine samples compared to unweighted UniFrac distance between combined freshwater and combined marine samples for each phylum and proteobacterial class (a). Unweighted UniFrac distances between combined freshwater and combined marine samples for orders (b) and families (c) within each phylum/class. Phyla, classes, orders, and families are included in the analysis if they occurred in at least 3 freshwater and 3 marine samples and contained at least 5 nodes. Download FIG S3, EPS file, 0.3 MB.

    Copyright © 2018 Paver et al.

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

  • TABLE S1

    UniFrac distance calculated between marine and freshwater sequences for each family. Download Table S1, PDF file, 0.04 MB.

    Copyright © 2018 Paver et al.

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

  • FIG S4

    Phylogenetic trees of select phyla and proteobacterial classes: (A) Alphaproteobacteria, (B) Actinobacteria, (C) Betaproteobacteria, (D) Chloroflexi. External ring colors indicate the habitats where MED nodes were detected in the data set: freshwater (green), marine (blue), both (orange). Notable clades are indicated by colored wedges. Download FIG S4, EPS file, 1.6 MB.

    Copyright © 2018 Paver et al.

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

  • FIG S5

    Fraction of freshwater nodes shared with marine systems as a function of freshwater sites sampled (a) and fraction of marine nodes shared with freshwater systems as a function of marine sites sampled (b). Download FIG S5, EPS file, 0.4 MB.

    Copyright © 2018 Paver et al.

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

  • FIG S6

    As sequence identity cutoff value increases, more taxa are shared between marine-freshwater sample pairs. Decrease in Jaccard index between marine-freshwater sample pairs (unshared taxa)/(shared taxa) with increasing sequence similarity cutoff values for Alphaproteobacteria and Verrucomicrobia (a). Example phylogenetic trees are shown for groups with high sequence similarity (b) and low sequence similarity (c) between marine (blue) and freshwater (green) samples. Download FIG S6, EPS file, 0.9 MB.

    Copyright © 2018 Paver et al.

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

  • FIG S7

    Minimum sequence identity threshold (i.e., finest-scale resolution) at which pairs of marine and freshwater samples share common taxa. In contrast to Fig. 2, this analysis used a data set where sequences were preclustered to allow up to 2 base pair differences within a sequence group. Box plots indicate the median, quartiles, and range of values observed for all marine-freshwater sample pairs. A heat map illustrates the number of freshwater (F) and marine (M) samples containing representatives of each phylum/proteobacterial class. Download FIG S7, EPS file, 0.4 MB.

    Copyright © 2018 Paver et al.

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

  • FIG S8

    Neighbor-joining consensus tree of nucleotide sequences (a) and nucleotide and protein alignment (b) of partial genes from the protein cluster identified as COG2609 (pyruvate dehydrogenase complex, dehydrogenase E1 component). Strain names are colored based on phylogenetic classification within the SAR11 clade: green, LD12 sequences from group IIIb; light blue, group IIIa, sister group to IIIb; blue, all other marine SAR11 clades included in the analysis (Ia, II); black, a sequence read from the Lake Erie metagenome identified by pplacer as marine SAR11. Consensus support values (%) are indicated on tree branches (a). Vertical boxes have been added to the alignment to indicate amino acids where the Great Lakes sequence contains shared characters with a subset of included strains. Download FIG S8, JPG file, 0.8 MB.

    Copyright © 2018 Paver et al.

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

  • TABLE S2

    Additional information on 16S rRNA tag sequencing data sets compiled for the meta-analysis. Download Table S2, PDF file, 0.1 MB.

    Copyright © 2018 Paver et al.

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

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Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems
Sara F. Paver, Daniel Muratore, Ryan J. Newton, Maureen L. Coleman
mSystems Nov 2018, 3 (6) e00232-18; DOI: 10.1128/mSystems.00232-18

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Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems
Sara F. Paver, Daniel Muratore, Ryan J. Newton, Maureen L. Coleman
mSystems Nov 2018, 3 (6) e00232-18; DOI: 10.1128/mSystems.00232-18
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    • ABSTRACT
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KEYWORDS

16S rRNA
SAR11
aquatic ecology
aquatic microbiology
biogeography
environmental transitions
microbial ecology
tag sequencing

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