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Award Abstract # 1737409
Protistan, prokaryotic, and viral processes at the San Pedro Ocean Time-series

NSF Org: OCE
Division Of Ocean Sciences
Recipient: UNIVERSITY OF SOUTHERN CALIFORNIA
Initial Amendment Date: July 11, 2017
Latest Amendment Date: July 11, 2017
Award Number: 1737409
Award Instrument: Standard Grant
Program Manager: Cynthia Suchman
csuchman@nsf.gov
 (703)292-2092
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: August 1, 2017
End Date: July 31, 2023 (Estimated)
Total Intended Award Amount: $1,528,834.00
Total Awarded Amount to Date: $1,528,834.00
Funds Obligated to Date: FY 2017 = $1,528,834.00
History of Investigator:
  • Jed Fuhrman (Principal Investigator)
    fuhrman@usc.edu
  • David Caron (Co-Principal Investigator)
Recipient Sponsored Research Office: University of Southern California
3720 S FLOWER ST FL 3
LOS ANGELES
CA  US  90033
(213)740-7762
Sponsor Congressional District: 34
Primary Place of Performance: University of Southern California
3616 Trousdale Parkway, AHF 211
Los Angeles
CA  US  90089-0371
Primary Place of Performance
Congressional District:
37
Unique Entity Identifier (UEI): G88KLJR3KYT5
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001718DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 8811, 9117
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Planktonic marine microbial communities consist of a diverse collection of bacteria, archaea, viruses, protists (phytoplankton and protozoa) and small animals (metazoan). Collectively, these species are responsible for virtually all marine pelagic primary production where they form the basis of food webs and carry out a large fraction of respiratory processes. Microbial interactions include the traditional role of predation, but recent research recognizes the importance of parasitism, symbiosis and viral infection. Characterizing the response of pelagic microbial communities and processes to environmental influences is fundamental to understanding and modeling carbon flow and energy utilization in the ocean, but very few studies have attempted to study all of these assemblages in the same study. This project is comprised of long-term (monthly) and short-term (daily) sampling at the San Pedro Ocean Time-series (SPOT) site. Analysis of the resulting datasets investigates co-occurrence patterns of microbial taxa (e.g. protist-virus and protist-prokaryote interactions, both positive and negative) indicating which species consistently co-occur and potentially interact, followed by examination gene expression to help define the underlying mechanisms. This study augments 20 years of baseline studies of microbial abundance, diversity, rates at the site, and will enable detection of low-frequency changes in composition and potential ecological interactions among microbes, and their responses to changing environmental forcing factors. These responses have important consequences for higher trophic levels and ocean-atmosphere feedbacks. The broader impacts of this project include training graduate and undergraduate students, providing local high school student with summer lab experiences, and PI presentations at local K-12 schools, museums, aquaria and informal learning centers in the region. Additionally, the PIs advise at the local, county and state level regarding coastal marine water quality.

This research project is unique in that it is a holistic study (including all microbes from viruses to small metazoa) of microbial species diversity and ecological activities, carried out at the SPOT site off the coast of southern California. In studying all microbes simultaneously, this work aims to identify important ecological interactions among microbial species, and identify the basis(es) for those interactions. This research involves (1) extensive analyses of prokaryote (archaean and bacterial) and eukaryote (protistan and micro-metazoan) diversity via the sequencing of marker genes, (2) studies of whole-community gene expression by eukaryotes and prokaryotes in order to identify key functional characteristics of microorganismal groups and the detection of active viral infections, and (3) metagenomic analysis of viruses and bacteria to aid interpretation of transcriptomic analyses using genome-encoded information. The project includes exploratory metatranscriptomic analysis of poorly-understood aphotic and hypoxic-zone protists, to examine their stratification, functions and hypothesized prokaryotic symbioses.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 15)
Caron, David A. and Hu, Sarah K. "Are We Overestimating Protistan Diversity in Nature?" Trends in Microbiology , v.27 , 2019 10.1016/j.tim.2018.10.009 Citation Details
Gleich, Samantha J. and Cram, Jacob A. and Weissman, Jake L. and Caron, David A. "NetGAM: Using generalized additive models to improve the predictive power of ecological network analyses constructed using time-series data" ISME Communications , v.2 , 2022 https://doi.org/10.1038/s43705-022-00106-7 Citation Details
Hu, Sarah K. and Liu, Zhenfeng and Alexander, Harriet and Campbell, Victoria and Connell, Paige E. and Dyhrman, Sonya T. and Heidelberg, Karla B. and Caron, David A. "Shifting metabolic priorities among key protistan taxa within and below the euphotic zone: Depth-related protistan metatranscriptomes" Environmental Microbiology , v.20 , 2018 10.1111/1462-2920.14259 Citation Details
Ignacio-Espinoza, J. Cesar and Ahlgren, Nathan A. and Fuhrman, Jed A. "Long-term stability and Red Queen-like strain dynamics in marine viruses" Nature Microbiology , v.5 , 2020 10.1038/s41564-019-0628-x Citation Details
Leles, Suzana Gonçalves and Mitra, Aditee and Flynn, Kevin John and Tillmann, Urban and Stoecker, Diane and Jeong, Hae Jin and Burkholder, JoAnn and Hansen, Per Juel and Caron, David A. and Glibert, Patricia M. and Hallegraeff, Gustaaf and Raven, John A. "Sampling bias misrepresents the biogeographical significance of constitutive mixotrophs across global oceans: XXXX" Global Ecology and Biogeography , v.28 , 2019 10.1111/geb.12853 Citation Details
Long, Andrew M. and Hou, Shengwei and Ignacio-Espinoza, J. Cesar and Fuhrman, Jed A. "Benchmarking microbial growth rate predictions from metagenomes" The ISME Journal , v.15 , 2020 https://doi.org/10.1038/s41396-020-00773-1 Citation Details
McNichol, Jesse and Berube, Paul M. and Biller, Steven J. and Fuhrman, Jed A. "Evaluating and Improving Small Subunit rRNA PCR Primer Coverage for Bacteria, Archaea, and Eukaryotes Using Metagenomes from Global Ocean Surveys" mSystems , v.6 , 2021 https://doi.org/10.1128/mSystems.00565-21 Citation Details
Ollison, Gerid A. and Hu, Sarah K. and Hopper, Julie V. and Stewart, Brittany P. and Smith, Jayme and Beatty, Jennifer L. and Rink, Laura K. and Caron, David A. "Daily dynamics of contrasting spring algal blooms in Santa Monica Bay (central Southern California Bight)" Environmental Microbiology , 2022 https://doi.org/10.1111/1462-2920.16137 Citation Details
Sieradzki, Ella T. and Ignacio-Espinoza, J. Cesar and Needham, David M. and Fichot, Erin B. and Fuhrman, Jed A. "Dynamic marine viral infections and major contribution to photosynthetic processes shown by spatiotemporal picoplankton metatranscriptomes" Nature Communications , v.10 , 2019 10.1038/s41467-019-09106-z Citation Details
Sieradzki, Ella T. and Morando, Michael and Fuhrman, Jed A. "Metagenomics and Quantitative Stable Isotope Probing Offer Insights into Metabolism of Polycyclic Aromatic Hydrocarbon Degraders in Chronically Polluted Seawater" mSystems , v.6 , 2021 https://doi.org/10.1128/mSystems.00245-21 Citation Details
Weissman, Jake L. and Hou, Shengwei and Fuhrman, Jed A. "Estimating maximal microbial growth rates from cultures, metagenomes, and single cells via codon usage patterns" Proceedings of the National Academy of Sciences , v.118 , 2021 https://doi.org/10.1073/pnas.2016810118 Citation Details
(Showing: 1 - 10 of 15)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

This project constituted an extension of our long-term microbial plankton time series in the San Pedro Channel, located roughly midway between Los Angeles and Santa Catalina Island, in open water about 20 km offshore (and depths from the surface to the bottom), to now cover 23 years of monthly observations. This latest grant also supported daily time series analyses from coastal water by the local Santa Monica Pier. The organisms we have been studying include bacteria, archaea, eukaryotes, and viruses, making this study unusually comprehensive and capable of discerning patterns not previously recognized. This is particularly valuable considering that this collection of microorganisms is responsible for the large majority of marine productivity and its consumption. Much of the work involved analyses of DNA (from the genomes of all the organisms, collectively called the metagenome) and RNA (transcripts of all the genes being expressed, also known as the metatranscriptome). As part of this study we validated our community composition analyses with carefully curated mock communities. Among the intellectually meritorious outcomes were observations that the bacterial and archaeal communities were much more stable over months and years than were the eukaryotic communities, though both showed seasonal patterns. The eukaryotic phytoplankton (producers) were more stable than eukaryotic heterotrophs (consumers). Bacteria and archaea made up a surprisingly large proportion of the organisms in the size fraction we had thought would be more dominated by protists (they constituted 40-90% of the ribosomal RNA marker genes in the > 1 micrometer size fraction). We also determined that during the warm El Nino years 2014-2015, there was a community shift where the summer microbial community occurred year-round instead of having the usual shift to a winter community in that season. Interestingly, during that warm period, a particular type of Prochlorococcus cyanobacterium appeared at our study site, having not been seen there over the decade before, but one that usually lives in tropical areas. These shifts in communities provide direct evidence of what kinds of changes to expect in a warming world. Our studies also determined previously unrecognized diversity patterns with ocean depth, notably that prokaryotic (bacterial and archaeal) diversity peaked at mid-depths while the protistan diversity peaked at the surface.  In studies of microbial interactions, we found that DNA viruses were particularly important in controlling the free-living bacterial community composition while phytoplankton were most important in controlling the particle-attached bacterial community. Our daily time series studies at Santa Monica Pier provided major insights into the conditions that lead to different kinds of algal blooms, in that we were lucky to observe blooms of both diatoms and dinoflagellates, the two guilds of phytoplankton that yield most large algal blooms globally. In metatranscriptional time series studies, we found that diatoms, which bloomed following upwelling events, expressed an array of gene categories related to dissolved inorganic nitrogen utilization, and genes related to the catabolism of chitin that may have prolonged their bloom duration following nitrogen depletion. Conversely, dinoflagellates bloomed under less-replete inorganic nitrogen conditions, exhibited less variation in transcriptional activity, and expressed few gene categories associated with dissolved inorganic nutrients during their bloom. Dinoflagellate profiles exhibited evidence of proteolysis and heterotrophy that may have enabled them to circumvent nutrient limitation and bloom to high abundances. Taken together, diatom and dinoflagellate transcriptional profiles illustrated guild-specific physiology, tuned to respond to and thrive under distinct environmental windows of opportunity.  Broader impacts of the study include showcasing our work on our websites as well as supporting a significant education and training component of several early-career marine scientists (PhD students, Masters students, technicians), undergraduate students (from USC and elsewhere as part of a REU program) and students from Los-Angeles area high schools and colleges.

 


Last Modified: 11/22/2023
Modified by: Jed A Fuhrman

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