Macrofaunal control of microbial community structure in continental margin sediments

Abstract

Through a process called "bioturbation," burrowing macrofauna have altered the seafloor habitat and modified global carbon cycling since the Cambrian. However, the impact of macrofauna on the community structure of microorganisms is poorly understood. Here, we show that microbial communities across bioturbated, but geochemically and sedimentologically divergent, continental margin sites are highly similar but differ clearly from those in nonbioturbated surface and underlying subsurface sediments. Solid- and solute-phase geochemical analyses combined with modeled bioturbation activities reveal that dissolved O₂ introduction by burrow ventilation is the major driver of archaeal community structure. By contrast, solid-phase reworking, which regulates the distribution of fresh, algal organic matter, is the main control of bacterial community structure. In nonbioturbated surface sediments and in subsurface sediments, bacterial and archaeal communities are more divergent between locations and appear mainly driven by site-specific differences in organic carbon sources.

Keywords: bioturbation; burrow ventilation; organic carbon sources; particle reworking; redox state.

Fig. 1.

Geochemical characterizations and indicators of bioturbation activity at AU1 to AU4. (A) Depth profiles of SO₄²⁻, CH₄, DIC, TOC, δ¹³C-TOC, and C:N ratios across the entire cored intervals. Ventilation-dominated layers (VLs), reworking-dominated layers (RLs), and sulfate–methane transitions (SMTs) are indicated by horizontal dashed, solid, and dotted lines, respectively. (B) Bioturbation activities indicated by profiles of chl a, modeled rates of biodiffusional mixing (D_B), nonlocal mixing (N_a), and bioirrigation (α), as well as % Fe(III) in the top 0 to 40 cm. (C) Composition of macrofaunal communities, based on counts of individuals.

Fig. 2.

Depth profiles of microbial communities at AU1 to AU4. (A) 16S rRNA gene abundances of Bacteria and Archaea (red triangles, Bacteria; blue diamonds, Archaea); (B) Bacteria-to-Archaea ratios (BARs); (C) Chao1 richness of Bacteria and Archaea; (D and E) community compositions of Bacteria and Archaea. The VLs, RLs, and SMTs are indicated by horizontal dashed, solid, and dotted lines, respectively. The black arrows indicate local peaks in chl a or excess ²¹⁰Pb from Fig. 1.

Fig. 3.

Ordination analyses of microbial community composition and its environmental drivers. (A) PCoA plots of bacterial and archaeal communities based on weighted Unifrac distances. Clusters consisting of samples from VLs, RLs, and nonbioturbated layers are shaded in deep blue, light blue, and red, respectively. Intercluster dissimilarities analyzed by PERMANOVA were highly significant (P < 0.001) in all cases. (B) Relationships between microbial communities and environmental variables examined by CAP. The asterisks indicate significance levels based on PERMANOVA (***P < 0.001; **P < 0.01).

Fig. 4.

Depth profiles of 18S rRNA gene abundances and community composition. Photosynthetic lineages, i.e., Bacillariophyta, Dinoflagellata, Chlorophyta, and Streptophyta, are indicated by green colors.

Fig. 5.

Conceptual path model to investigate the relationships between bioturbation activity, sediment biogeochemistry, and microbial and eukaryotic community structure: (A) surface sediments (0 to 40 cm) and (B) subsurface sediments (>40 cm). The red and blue colors distinguish solid-phase (D_B, N_a) and solute-phase (α) bioturbation parameters. All calculations are based on PLS regression, VPA-RDA, and Mantel test. Widths of arrows and wave lines are proportional to the explanatory power of VPA-RDA variables and Mantel coefficients, respectively. ***P < 0.001; **P < 0.01; *P < 0.5. Note: Surface and subsurface sediments are divided at 40 cm based on Fig. 1. Changing this division to other depths does not significantly alter the statistical outcomes, however (SI Appendix, Fig. S9).

Fig. 6.

Pairwise Spearman correlations of relative abundances of (A) bacterial and (B) archaeal lineages with environmental variables and relative abundances of dominant eukaryotic groups. Only significant (P < 0.05) correlations are shown. The asterisks mark which environmental variable shows the strongest correlation with each given microbial lineage. Note: Correlations of α, %Fe(III), D_B, N_a, and chl a with microbial lineages were only calculated for surface sediment where data exist for both.