TY - JOUR
T1 - Ecophysiology of uncultivated marine euryarchaea is linked to particulate organic matter
AU - Orsi, William D.
AU - Smith, Jason M.
AU - Wilcox, Heather M.
AU - Swalwell, Jarred E.
AU - Carini, Paul
AU - Worden, Alexandra Z.
AU - Santoro, Alyson E.
N1 - Funding Information:
We thank the captain and crew of the Monterey Bay Aquarium Research Institute (MBARI) vessel R/V Western Flyer during cruises CN207, C0912 and CN13ID. We thank Valeria Jimenez, Noriko Okamoto, Tim Pennington and Marguerite Blum for assistance with sample collection at sea, Sebastian Sudek for preparing the M. pusilla culture, and Francisco Chavez, chief scientist on cruise C0912. We thank the MBARI Biological Oceanography Group for Chl a and dissolved nutrient data, Christopher Francis for use of the barcoded amplicon data, and Nicholas Nidzieko for assistance with ocean color data. We thank Laurence P Madin for discussions about tunicate and Salpa physiology, Amy Apprill for advice and information about amplicon libraries, and Patrick Keeling and Thomas Richards for helpful discussions throughout the project. This work was funded by the Gordon and Betty Moore Foundation through grants GBMF3307 to AES and AZW, GBMF1668 to AZW, National Science Foundation Grants OCE-1260006 and DBI-1318455 to AES, and the David and Lucile Packard Foundation (in support of cruises as well as JMS, HMW, JES and AZW contributions). This is University of Maryland Center for Environmental Science contribution 4919.
Publisher Copyright:
© 2015 International Society for Microbial Ecology. All rights reserved.
PY - 2015/8/23
Y1 - 2015/8/23
N2 - Particles in aquatic environments host distinct communities of microbes, yet the evolution of particlespecialized taxa and the extent to which specialized microbial metabolism is associated with particles is largely unexplored. Here, we investigate the hypothesis that a widely distributed and uncultivated microbial group - the marine group II euryarchaea (MGII) - interacts with living and detrital particulate organic matter (POM) in the euphotic zone of the central California Current System. Using fluorescent in situ hybridization, we verified the association of euryarchaea with POM. We further quantified the abundance and distribution of MGII 16S ribosomal RNA genes in size-fractionated seawater samples and compared MGII functional capacity in metagenomes from the same fractions. The abundance of MGII in free-living and <3 μm fractions decreased with increasing distance from the coast, whereas MGII abundance in the 0.8-3 lm fraction remained constant. At several offshore sites, MGII abundance was highest in particle fractions, indicating that particle-attached MGII can outnumber free-living MGII under oligotrophic conditions. Compared with free-living MGII, the genome content of MGII in particleassociated fractions exhibits an increased capacity for surface adhesion, transcriptional regulation and catabolism of high molecular weight substrates. Moreover, MGII populations in POM fractions are phylogenetically distinct from and more diverse than free-living MGII. Eukaryotic phytoplankton additions stimulated MGII growth in bottle incubations, providing the first MGII net growth rate measurements. These ranged from 0.47 to 0.54 d-1. However, MGII were not recovered in wholegenome amplifications of flow-sorted picoeukaryotic phytoplankton and heterotrophic nanoflagellates, suggesting that MGII in particle fractions are not physically attached to living POM. Collectively, our results support a linkage between MGII ecophysiology and POM, implying that marine archaea have a role in elemental cycling through interactions with particles.
AB - Particles in aquatic environments host distinct communities of microbes, yet the evolution of particlespecialized taxa and the extent to which specialized microbial metabolism is associated with particles is largely unexplored. Here, we investigate the hypothesis that a widely distributed and uncultivated microbial group - the marine group II euryarchaea (MGII) - interacts with living and detrital particulate organic matter (POM) in the euphotic zone of the central California Current System. Using fluorescent in situ hybridization, we verified the association of euryarchaea with POM. We further quantified the abundance and distribution of MGII 16S ribosomal RNA genes in size-fractionated seawater samples and compared MGII functional capacity in metagenomes from the same fractions. The abundance of MGII in free-living and <3 μm fractions decreased with increasing distance from the coast, whereas MGII abundance in the 0.8-3 lm fraction remained constant. At several offshore sites, MGII abundance was highest in particle fractions, indicating that particle-attached MGII can outnumber free-living MGII under oligotrophic conditions. Compared with free-living MGII, the genome content of MGII in particleassociated fractions exhibits an increased capacity for surface adhesion, transcriptional regulation and catabolism of high molecular weight substrates. Moreover, MGII populations in POM fractions are phylogenetically distinct from and more diverse than free-living MGII. Eukaryotic phytoplankton additions stimulated MGII growth in bottle incubations, providing the first MGII net growth rate measurements. These ranged from 0.47 to 0.54 d-1. However, MGII were not recovered in wholegenome amplifications of flow-sorted picoeukaryotic phytoplankton and heterotrophic nanoflagellates, suggesting that MGII in particle fractions are not physically attached to living POM. Collectively, our results support a linkage between MGII ecophysiology and POM, implying that marine archaea have a role in elemental cycling through interactions with particles.
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U2 - 10.1038/ismej.2014.260
DO - 10.1038/ismej.2014.260
M3 - Article
C2 - 25615436
AN - SCOPUS:84937728907
SN - 1751-7362
VL - 9
SP - 1747
EP - 1763
JO - ISME Journal
JF - ISME Journal
IS - 8
ER -