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

Jacqueline Comstock; Lillian C Henderson; Hilary G Close; Shuting Liu; Kevin Vergin; Alexandra Z Worden; Fabian Wittmers; Elisa Halewood; Stephen Giovannoni; Craig A Carlson

doi:10.1093/ismeco/ycae090

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

ISME Commun. 2024 Jul 12;4(1):ycae090. doi: 10.1093/ismeco/ycae090. eCollection 2024 Jan.

Authors

Jacqueline Comstock¹, Lillian C Henderson², Hilary G Close², Shuting Liu^{1

3}, Kevin Vergin⁴, Alexandra Z Worden^{5

6}, Fabian Wittmers^{5

6}, Elisa Halewood¹, Stephen Giovannoni⁴, Craig A Carlson¹

Affiliations

¹ Department of Ecology, Evolution and Marine Biology, Marine Science Institute, University of California Santa Barbara, Santa Barbara, CA 93106, United States.
² Department of Ocean Sciences, Rosenstiel School of Marine, Atmospheric, and Earth Science, University of Miami, Miami, FL 33149, United States.
³ Department of Environmental and Sustainability Sciences, Kean University, Union, NJ 07083, United States.
⁴ Department of Microbiology, Oregon State University, Corvallis, OR 97331, United States.
⁵ Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, MA 02543, United States.
⁶ Faculty of Mathematics and Natural Sciences, Christian-Albrecht University of Kiel, SH, 24118 Kiel, Germany.

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.