Effects of nutrient enrichment on surface microbial community gene expression in the oligotrophic North Pacific Subtropical Gyre

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Abstract

Marine microbial communities are critical for biogeochemical cycles and the productivity of ocean ecosystems. Primary productivity in the surface ocean is constrained by nutrients which are supplied, in part, by mixing with deeper water. Little is known about the time scales, frequency, or impact of mixing on microbial communities. We combined in situ sampling using the Environmental Sample Processor and a small-scale mixing experiment with lower euphotic zone water to determine how individual populations respond to mixing. Transcriptional responses were measured using the MicroTOOLs (Microbiological Targets for Ocean Observing Laboratories) microarray, which targets all three domains of life and viruses. The experiment showed that mixing substantially affects photosynthetic taxa as expected, but surprisingly also showed that populations respond differently to unfiltered deep water which contains particles (organisms and detritus) compared to filtered deep water that only contains nutrients and viruses, pointing to the impact of biological interactions associated with these events. Comparison between experimental and in situ population transcription patterns indicated that manipulated populations can serve as analogs for natural populations, and that natural populations may be frequently or continuously responding to nutrients from deeper waters. Finally, this study also shows that the microarray approach, which is complementary to metatranscriptomic sequencing, is useful for determining the physiological status of in situ microbial communities.

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Acknowledgements

The authors would like to thank the Center for Microbial Oceanography, Research and Education (C-MORE grant number EF0424599, J.Z. and D.M.K.), the Simons Collaboration on Ocean Processes and Ecology (a grant from the Simons Foundation – SCOPE Award ID 329108, J.Z. and D.M.K.), the David and Lucile Packard Foundation, the Gordon and Betty Moore Foundation MEGAMER Facilities Grant (number 1761 to J.Z.) and Investigator Award (number 3794 to D.M.K.) and National Science Foundation Dimensions of Biodiversity Program (grant number 1241221, J.Z.) for funding and resources. The expertise of the international MicroTOOLs Team was crucial in the development of a successful environmental microarray. The MicroTOOLs array hybridization was performed at the Roy J. Carver Center for Genomics, The University of Iowa, USA. Steve Poulos and Lance Fujieki kindly provided Seaglider density data and images. We also thank Ariel Rabines, Roman Marin III, John Ryan, Gene Massion, Blake Watkins, Mariona Segura-Noguera, Susan Curless and the captain and crew of the R/V Kilo Moana.

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Correspondence to J. P. Zehr.

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Robidart, J.C., Magasin, J.D., Shilova, I.N. et al. Effects of nutrient enrichment on surface microbial community gene expression in the oligotrophic North Pacific Subtropical Gyre. ISME J 13, 374–387 (2019) doi:10.1038/s41396-018-0280-0

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