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Single-cell view of deep-sea microbial activity and intracommunity heterogeneity

Abstract

Microbial activity in the deep sea is cumulatively important for global elemental cycling yet is difficult to quantify and characterize due to low cell density and slow growth. Here, we investigated microbial activity off the California coast, 50–4000 m water depth, using sensitive single-cell measurements of stable-isotope uptake and nucleic acid sequencing. We observed the highest yet reported proportion of active cells in the bathypelagic (up to 78%) and calculated that deep-sea cells (200–4000 m) are responsible for up to 34% of total microbial biomass synthesis in the water column. More cells assimilated nitrogen derived from amino acids than ammonium, and at higher rates. Nitrogen was assimilated preferentially to carbon from amino acids in surface waters, while the reverse was true at depth. We introduce and apply the Gini coefficient, an established equality metric in economics, to quantify intracommunity heterogeneity in microbial anabolic activity. We found that heterogeneity increased with water depth, suggesting a minority of cells contribute disproportionately to total activity in the deep sea. This observation was supported by higher RNA/DNA ratios for low abundance taxa at depth. Intracommunity activity heterogeneity is a fundamental and rarely measured ecosystem parameter and may have implications for community function and resilience.

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Fig. 1: Sampling location and dissimilarities in the microbial community composition between samples.
Fig. 2: Proportion of active microbial cells with water depth.
Fig. 3: Magnitude and distribution of microbial activity.
Fig. 4: Boxplot of C/N relative use efficiency in cells assimilating both C and N from amino acids.
Fig. 5: Intracommunity heterogeneity in microbial anabolic activity.
Fig. 6: Average RNA/DNA ratio for ASVs divided into DNA relative abundance quartiles by depth, integrated between all study sites.

Data availability

The authors declare that all data supporting the findings of this study are available within the article and its Supplementary Information file, or from the corresponding author upon request. All sequences have been submitted to the European Nucleotide Archive (ENA) under the project accession number PRJEB54878.

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Acknowledgements

This work was supported the Simons Foundation (Early Career Investigator Award 507798 to AED). The cruise on the R/V Oceanus was supported by the National Science Foundation (OCE-1634297 to AED). We thank the captain and crew of OC1703A for their support during the fieldwork, and Julian Fortney, Bennett Kapili and Nicolette Meyer for their help during sample collection. The nanoSIMS analyses were performed at the Stanford Nano Shared Facilities (SNSF), supported by the National Science Foundation under award ECCS-2026822. We thank Christie Jilly-Rehak and Chuck Hitzman at the SNSF for their support during the nanoSIMS analysis.

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AEP and AED collected samples and designed and conducted the stable isotope experiment. AEP performed nutrient analyses. NAG performed DNA/RNA preparation for sequencing and nanoSIMS measurements. NAG analyzed the data and generated the figures. NAG and AED interpreted the data and wrote the paper with input from AEP.

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Correspondence to N. Arandia-Gorostidi or A. E. Dekas.

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Arandia-Gorostidi, N., Parada, A.E. & Dekas, A.E. Single-cell view of deep-sea microbial activity and intracommunity heterogeneity. ISME J (2022). https://doi.org/10.1038/s41396-022-01324-6

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