Abstract
Dissolved organic nitrogen (DON) supports a significant amount of heterotrophic production in the ocean. Yet, to date, the identity and diversity of microbial groups that transform DON are not well understood. To better understand the organisms responsible for transforming high molecular weight (HMW)-DON in the upper ocean, isotopically labeled protein extract from Micromonas pusilla, a eukaryotic member of the resident phytoplankton community, was added as substrate to euphotic zone water from the central California Current system. Carbon and nitrogen remineralization rates from the added proteins ranged from 0.002 to 0.35 μmol C l−1 per day and 0.03 to 0.27 nmol N l−1 per day. DNA stable-isotope probing (DNA-SIP) coupled with high-throughput sequencing of 16S rRNA genes linked the activity of 77 uncultivated free-living and particle-associated bacterial and archaeal taxa to the utilization of Micromonas protein extract. The high-throughput DNA-SIP method was sensitive in detecting isotopic assimilation by individual operational taxonomic units (OTUs), as substrate assimilation was observed after only 24 h. Many uncultivated free-living microbial taxa are newly implicated in the cycling of dissolved proteins affiliated with the Verrucomicrobia, Planctomycetes, Actinobacteria and Marine Group II (MGII) Euryarchaeota. In addition, a particle-associated community actively cycling DON was discovered, dominated by uncultivated organisms affiliated with MGII, Flavobacteria, Planctomycetes, Verrucomicrobia and Bdellovibrionaceae. The number of taxa assimilating protein correlated with genomic representation of TonB-dependent receptor (TBDR)-encoding genes, suggesting a possible role of TBDR in utilization of dissolved proteins by marine microbes. Our results significantly expand the known microbial diversity mediating the cycling of dissolved proteins in the ocean.
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Acknowledgements
We thank the captain and crew of the R/V Western Flyer, J. Timothy Pennington, Marguerite Blum, Valeria Jimenez, Christopher Wahl, Noriko Okamoto, Jarred Swalwell and Francisco Chavez for logistical assistance prior to and during the cruise. We also thank Michael Morando and Elizabeth Kujawinski for advice and conversations on SIP methodology, and Mak Saito and Dawn Moran for advice on for protein extraction. We thank Amy Apprill for sharing the modified, barcoded PCR primers, Alexandra Welch for assistance with qPCR, and Paul Carini and Tristan Horner for discussions. We thank John Hobbie for discussions on protein remineralization rate kinetics, and three anonymous reviewers for their helpful comments. Support for this work was provided by GBMF3307 to PJK, TAR, AZW and AES, United States National Science Foundation award DBI-1318455 to AES, and the David and Lucile Packard Foundation (to AZW). This is UMCES contribution number 5169.
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Orsi, W., Smith, J., Liu, S. et al. Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean. ISME J 10, 2158–2173 (2016). https://doi.org/10.1038/ismej.2016.20
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