Marine particle size-fractionation indicates organic matter is processed by differing microbial communities on depth-specific particles

Abstract

Passive sinking flux of particulate organic matter in the ocean plays a central role in the biological carbon pump and carbon export to the ocean's interior. Particle-associated microbes colonize particulate organic matter, producing "hotspots" of microbial activity. We evaluated variation in particle-associated microbial communities to 500 m depth across four different particle size fractions (0.2-1.2, 1.2-5, 5-20, >20 μm) collected using in situ pumps at the Bermuda Atlantic Time-series Study site. In situ pump collections capture both sinking and suspended particles, complementing previous studies using sediment or gel traps, which capture only sinking particles. Additionally, the diagenetic state of size-fractionated particles was examined using isotopic signatures alongside microbial analysis. Our findings emphasize that different particle sizes contain distinctive microbial communities, and each size category experiences a similar degree of change in communities over depth, contradicting previous findings. The robust patterns observed in this study suggest that particle residence times may be long relative to microbial succession rates, indicating that many of the particles collected in this study may be slow sinking or neutrally buoyant. Alternatively, rapid community succession on sinking particles could explain the change between depths. Complementary isotopic analysis of particles revealed significant differences in composition between particles of different sizes and depths, indicative of organic particle transformation by microbial hydrolysis and metazoan grazing. Our results couple observed patterns in microbial communities with the diagenetic state of associated organic matter and highlight unique successional patterns in varying particle sizes across depth.

Keywords: 16S amplicon sequencing; Bermuda Atlantic Time-series Study; biological carbon pump; biological oceanography; marine microbiology; marine snow; particle-associated microbes; particulate organic matter.

Figure 1

(A) Separation of bulk δ¹⁵N values between fractions was observed below the DCM. (B) TP of particles was highest in the >20 μm fraction across all depths. (C) δ¹⁵N values threonine (Thr) normalized to δ¹⁵N values of phenylalanine (Phe) for POM size fractions show differing composition between size fractions. For comparison, the range of values found in phytoplankton and zooplankton fecal pellet end-members characterized by Doherty et al. (2021) are indicated by gray bars at the top. Additional comparison to end-members can be found in Fig. S7. Error bars indicate propagated analytical uncertainty. Samples were taken from July 2018.

Figure 2

NMDS ordinations show strong differences in microbial community composition are observed between fraction and depth. NMDS ordinations use bray-Curtis dissimilarities from 16S rRNA gene amplicon community composition, with Cyanobacteria and plastid sequences excluded. Shapes denote size fraction. Colors denote (A) depth within the water column and (B) time of collection.

Figure 3

A lower percentage of ASVs overlap between fractions below the UE. Venn diagrams show unique and overlapping ASVs between the 0.2–1.2, 1.2–5, 5–20, and >20 μm size fractions in (A) the UE, (B) the DCM, and (C) the twilight zone.

Figure 4

There is a low percentage of overlap between ASVs in the UE and the DCM or twilight zone. Venn diagrams show unique and overlapping amplicon sequence variants (ASVs) between depth bins associated with the UE, the DCM, and the twilight zone in (A) the 0.2–1.2 μm size fraction, (B) the 1.2–5 μm fraction, (C) the 5–20 μm fraction, and (D) the >20 μm fraction.

Figure 5

Significant differences in alpha diversity of the prokaryotic community based on 16S rRNA gene amplicons (excluding cyanobacteria and plastids) were observed between depth bins and timepoints in all size fractions.

Figure 6

Certain cyanobacterial ASVs demonstrated a higher relative abundance in larger fractions directly below their free-living max depths range. Boxes denote depths where Cyanobacteria are found with greater relative abundance in the PA size fractions compared to free-living fractions.

Figure 7

Average relative abundances of microbial taxa (including Cyanobacteria) grouped by order across size fractions and depth bins. Orders that comprised <1% of community composition were excluded from visualization.