Research ArticleMarine Ecology

Hypoxia causes preservation of labile organic matter and changes seafloor microbial community composition (Black Sea)

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Science Advances  10 Feb 2017:
Vol. 3, no. 2, e1601897
DOI: 10.1126/sciadv.1601897
  • Fig. 1 Study area (inset, star) and section of the outer northwestern Crimean shelf showing the position of sampling sites (inverted triangles).

    The filled areas show the minimum and maximum bottom-water oxygen or sulfide concentrations measured at different times between 25 April 2010 and 7 May 2010 (n = 128; measured between 0.05 and 12 m above seafloor). Blue, oxic; yellow, hypoxic; red-orange, anoxic-sulfidic conditions. The dashed line depicts the hypoxia threshold (63 μM O2).

  • Fig. 2 Sediment organic matter content and benthic fluxes.

    Surface sediments sampled by coring and respective percentage of organic carbon and chlorophyll a (Chl a) concentration downcore (y axis is depth in cm; core pictures depict top 5 cm). The vertical line at ~1.6% Corg and ~3 μg gdw−1 Chl a depicts the lowest Corg and chlorophyll a contents in samples obtained, assumed to be the threshold for remineralization in the time frame of 40 years [based on 210Pb; (37)]. Benthic fluxes (37), including sulfate reduction rates, are in oxygen equivalents (1:2 transformation). Color code depicts oxygenation regimes.

  • Fig. 3 Bacterial community structure in surface sediments.

    (A) NMDS ordination plot (Bray-Curtis distance matrix) of ARISA profiles for the sampling stations for surface sediments (0 to 1 cm below sea floor). Different colors represent different oxygenation regimes: blue, stable oxic; yellow, variable oxic-hypoxic; orange, variable anoxic-hypoxic; red, stable anoxic. Stress, 0.18. (B) Relative sequence abundance of bacterial classes across oxygenation regimes detected by 454 NGS. (C) Most abundant bacterial families in different sediment horizons [depth layer in parentheses (cm)]. Note that the term “oxic” refers to bottom-water oxygen concentration and not oxygen content in the sediments.

  • Fig. 4 Path diagram for the final model examining causal effects between bottom-water oxygen concentration (exogenous variable) and the endogenous variables: Organic matter (Corg, chlorophyll a, and THAA), bioturbation, macrofaunal and meiofaunal diversity (based on inverse Simpson index), faunal and microbial aerobic and anaerobic respiration [from Lichtschlag et al. (37)], and bacterial diversity (based on inverse Simpson index from ARISA).

    Arrows (paths) indicate negative (red) or positive (blue) effects of bottom-water oxygen concentration, respectively, and numbers associated with arrows represent path coefficients. The goodness-of-fit index of the model was 0.75. *P < 0.05; **P < 0.01; ***P < 0.001. °P = 0.08, marginally significant trend.

  • Fig. 5 Conceptual diagram of ecosystem processes changing with bottom-water oxygen on the northwestern Crimean shelf break (Black Sea).

    The filled areas (blue to red) show the minimum and maximum bottom-water oxygen or sulfide concentrations (see Fig. 1 for details) to which deposited organic matter (green circles) is exposed at the seafloor, leading to different remineralization rates. Diverse benthic communities inhabit the sediments, from fauna (macrofauna and meiofauna) to microbes, driving different functions in the ecosystem (see Fig. 4 for details on causal effects). Under stable oxic conditions, faunal abundance and bioturbation activity are high, leading to high aerobic respiration rates in all size classes (orange and yellow filled areas). At the onset of hypoxia, faunal respiration decreases and lack of bioturbation favors anaerobic microbial communities and processes such as sulfate reduction (purple filled area), increasing free hydrogen sulfide in pore waters of the subsurface layers and enhancing carbon preservation in anoxic sediments.

  • Table 1 Biogeochemistry of surface sediments (0 to 1 cm).

    Methane was around 1 to 2 nM, sulfate concentrations ranged between 13 and 17 μM, and molar organic carbon to nitrogen ratio was between 9.3 and 11.4 (mol/mol), without a specific trend (not shown). Values represent average and SD (n = 3) when available. In the case of acridine orange direct count (AODC), SD is based on counts of >100 squares on two replicate filters. Only oxic stations presented signs of bioturbation based on fauna abundances, shape of oxygen profiles, and microtopography [see Lichtschlag et al. (37) for details]. Range for faunal abundances is based on three to six replicate samples [integrated over the upper 5 cm; (37)]. Corg, organic carbon; Corg:N, molar Corg/N ratio; CPE, chloroplast pigment equivalents; THAA, surface and integrated concentrations over 0 to 5 cm in square brackets; DI, THAA-based degradation index; SRR, sulfate reduction rate; AODC, total cell counts based on AODC; < d.l., value below detection limit.

    Station/
    PANGAEA
    event
    label
    Location
    (latitude/
    longitude)
    Water
    depth
    (m)
    Corg
    (%)
    Chlorophyll
    a
    (μg gdw−1)
    CPE
    (μg
    gdw−1)
    THAA
    (μmol
    gdw−1
    [mmol m−2])
    DIFe2+*
    (μM)
    PO43−*
    (μM)
    Sulfide
    (μM)
    SRR*
    (nmol
    ml−1
    day−1)
    AODC
    (109
    cells
    cm−3
    sediment)
    Macrofauna*
    (×103
    individuals
    m−2)
    Meiofauna*
    (×104
    individuals
    m−2)
    462
    MSM15/
    1_462-1
    44°49.45′N
    33°9.26′E
    1052.6 ±
    1.7
    11 ± 41916.0 ±
    4.2 (754)
    0.6 ±
    0.1
    843< d.l.<d.l.2.5 ± 0.25–6.7138–273.4
    459
    MSM15/
    1_459-1
    44°40.48′N
    33°5.53′E
    1202.9123715.7 (845)1.350.8199.5
    487
    MSM15/
    1_487-1
    44°38.78′N
    33°0.25′E
    1364.6 ±
    0.9
    26 ± 964 ± 1923.5 ±
    9.5 (796)
    1.1 ±
    0.3
    215< d.l.14 ± 82.2 ± 0.026.3–
    51.4
    172.2–226.3
    513
    MSM15/
    1_513-1
    44°37.87′N
    32°57.22′E
    1474.2348213.7 (730)1.72.4109.5
    393
    MSM15/
    1_393-1
    44°37.08′N
    32°53.48′E
    1645.3 ±
    0.5
    32 ± 286 ± 434.1 ±
    11.7 (773)
    1.3 ±
    0.1
    147< d.l.15 ±
    10
    1.9 ± 0.11.25.0
    506
    MSM15/
    1_506-1
    44°36.38′N
    32°52.72′E
    1713.8296623.4 (1396)1.70
    448
    MSM15/
    1_448-1
    44°35.84′N
    32°49.03′E
    2074.9 ±
    1.1
    41 ± 994 ± 1624.9 ± 3.4
    (1289)
    1.5 ±
    0.5
    < d.l.39283 ±
    45
    2.4 ± 0.400.13

    *Data from Lichtschlag et al. (37).

    †Total sulfide concentration from upper 2 cm.

    • Table 2 DOM composition in pore waters as obtained from Fourier transform ion cyclotron resonance mass spectrometry analysis (pooled pore-water volume from 0 to 10 cm).

      Molecular weight for the molecules detected ranged from 406 to 461. Hydrogen and oxygen to carbon ratio (intensity weight average) ranged from 1.2 to 1.3 and 0.4 to 0.5, respectively. AImod, aromaticity index; DBE, double-bond equivalents; total CHO, CHON, and CHOP, percentage of formulae containing carbon, hydrogen, and phosphorus; total S-bearing compounds, percentage of formulae containing sulfur-bearing compounds.

      DOC (μM)
      and extraction
      efficiency (%)
      TDN (μM)
      and extraction
      efficiency (%)
      DOC/TDN
      molar ratio
      Group of
      formulae
      No. of
      formulae
      AImodwaDBEwaTotal
      CHO
      Total
      CHON
      Total
      CHOP
      Total
      S-bearing
      compounds
      Oxic387 (51%)58 (12%)6.6Exclusive oxic6780.28.833452817
      Anoxic275 (80%)81 (10%)3.4Exclusive anoxic6260.39.314271257
      Common
      formulae
      52870.27.43739122

    Supplementary Materials

    • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/2/e1601897/DC1

      table S1. Percentage of shared and total number of OTUs and ANOSIM based on Bray-Curtis distance matrix between oxygenation conditions (based on ARISA profiles, upper-left corner of the table).

      table S2. Percentage of shared and total number of OTU0.03 (based on 454 NGS, without singletons) between stations.

      table S3. Pairwise comparisons based on OTU presence-absence (without singletons) between oxygenation regimes (at the OTU0.03 level) for the three key bacterial groups: Deltaproteobacteria (up), Gammaproteobacteria (center), and Flavobacteriia (down).

      table S4. Overview of 454 OTU sequences of relevant bacterial types responding to changes in bottom water oxygen concentration.

      table S5. Ranking of most abundant bacterial OTUs (without singletons) in decreasing order of their relative sequence abundance (in %) across all samples.

      table S6. Contribution (%) of each hypothesized relationship (path) to global explained variability [global R2; see Tenenhaus et al. (107) for details].

      table S7. Abundance of macrofauna and meiofauna taxa of the northwestern Crimean Shelf.

      fig. S1. Ten years (5 May 2000 to 5 May 2010) of satellite-based surface chlorophyll a concentration.

      fig. S2. Downcore organic carbon (%Corg) in the upper 70 cm comparing permanent oxic (station 462, 105 m) and anoxic (station 448, 207 m) conditions on the Crimean shelf.

      fig. S3. Downcore THAA concentrations (μmol gdw−1) and DI comparing permanent oxic (station 462, 105 m) and anoxic (station 448, 207 m) conditions on the Crimean shelf.

      fig. S4. THAA concentration integrated 0 to 5 cm (bars) and THAA surface concentrations (triangles).

      fig. S5. Sulfurization ratio calculated for molecular formulae detected in pore waters extracted from oxic (A) and anoxic conditions (B).

      fig. S6. Downcore cell abundances [single cells (×109) ml sediment−1], in the upper 30 cm, comparing oxygen regimes on the Crimean shelf.

      fig. S7. Ordination biplots generated by Correspondence Analysis (CA) of benthic communities retrieved on the Crimean shelf; (A) bacterial communities (based on ARISA fingerprinting), (B) meiofaunal and (C) macrofaunal abundances of each taxonomic group.

    • Supplementary Materials

      This PDF file includes:

      • table S1. Percentage of shared and total number of OTUs and ANOSIM based on Bray-Curtis distance matrix between oxygenation conditions (based on ARISA profiles, upper-left corner of the table).
      • table S2. Percentage of shared and total number of OTU0.03 (based on 454 NGS, without singletons) between stations.
      • table S3. Pairwise comparisons based on OTU presence-absence (without singletons) between oxygenation regimes (at the OTU0.03 level) for the three key bacterial groups: Deltaproteobacteria (up), Gammaproteobacteria (center), and Flavobacteriia (down).
      • table S4. Overview of 454 OTU sequences of relevant bacterial types responding to changes in bottom water oxygen concentration.
      • table S5. Ranking of most abundant bacterial OTUs (without singletons) in decreasing order of their relative sequence abundance (in %) across all samples.
      • table S6. Contribution (%) of each hypothesized relationship (path) to global explained variability global R2; see Tenenhaus et al. (107) for details.
      • table S7. Abundance of macrofauna and meiofauna taxa of the northwestern Crimean Shelf.
      • fig. S1. Ten years (5 May 2000 to 5 May 2010) of satellite-based surface chlorophyll a concentration.
      • fig. S2. Downcore organic carbon (%Corg) in the upper 70 cm comparing permanent oxic (station 462, 105 m) and anoxic (station 448, 207 m) conditions on the Crimean shelf.
      • fig. S3. Downcore THAA concentrations (μmol gdw−1) and DI comparing permanent oxic (station 462, 105 m) and anoxic (station 448, 207 m) conditions on the Crimean shelf.
      • fig. S4. THAA concentration integrated 0 to 5 cm (bars) and THAA surface concentrations (triangles).
      • fig. S5. Sulfurization ratio calculated for molecular formulae detected in pore waters extracted from oxic (A) and anoxic conditions (B).
      • fig. S6. Downcore cell abundances single cells (×109) ml sediment−1, in the upper 30 cm, comparing oxygen regimes on the Crimean shelf.
      • fig. S7. Ordination biplots generated by Correspondence Analysis (CA) of benthic communities retrieved on the Crimean shelf; (A) bacterial communities (based on ARISA fingerprinting), (B) meiofaunal and (C) macrofaunal abundances of each taxonomic group.

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