Award: OCE-1737258

Estuaries are critical hotspots for the processing of carbon (C) as it transits from land to the coastal ocean, but large gaps remain in our understanding of estuarine C cycling including the influence of intense phytoplankton blooms. These blooms are becoming increasingly common worldwide and have the potential to alter the role of estuaries in global C dynamics. The objective of this study was to assess the impact of intense blooms on C cycling in the York River Estuary (YRE), a tributary of Chesapeake Bay and site of intense phytoplankton blooms in both spring and summer. Surveys were conducted across the entire YRE over two years to characterize the major patterns of C cycling and associated microbial communities, and during intensive spring and summer blooms in the upper/mid and lower estuary, respectively. Bimonthly sampling over the entire YRE occurred during 2018-19 which was characterized by exceptionally high riverine discharge that delivered large amounts of carbon dioxide (CO2) and dissolved organic C (DOC) to the estuary, and resulted in short flushing times and low salinities. The YRE ecosystem was net heterotrophic during most of both years, with respiration exceeding photosynthesis, and thus a source of CO2 to the atmosphere. Conversely, the system was in metabolic balance or slightly autotrophic with photosynthesis exceeding respiration during the colder months, particularly during an unusually large spring bloom in 2019 driven by the high discharge. During these conditions the YRE switched to CO2 uptake due to cold water temperatures and bloom photosynthesis. High discharge in spring 2021 also led to an unusually large spring bloom, which also drove the system to net autotrophy and CO2 uptake. Incubations demonstrated that the water column was generally net autotrophic across the entire estuary and during all seasons, while the sediments were net heterotrophic at both deep channel and shallow shoal sites, also across the entire estuary and during all seasons. The high discharge in 2018-19 likely prevented the typical summer blooms of the dinoflagellates Margalefidinium polykrikoides and Alexandrium monilatum in the lower YRE, but they reappeared in 2020-21. These blooms had a marked effect on C cycling, with substantially lower CO2 within bloom patches compared to outside, indicating CO2 uptake within patches and release outside of patches. Rates of planktonic production and respiration were dramatically elevated within bloom patches, as were concentrations of DOC, suggesting release by the blooms. Net heterotrophy within sediments increased sharply following the bloom, suggesting respiration of deposited bloom C. Following the blooms, CO2 concentrations in the lower YRE increased, suggesting the system reverted to net heterotrophy and CO2 release as bloom C was respired. We also observed a novel microbial succession of ammonia-oxidizing archaea (AOA) and dinoflagellate species during the late summer blooms. Based on metabarcoding analysis of 16S and 18S rRNA genes, AOA abundance started to increase with M. polykrikoides blooms and reached the highest abundance (5% of relative abundance) in the transition period between the blooms of M. polykrikoides and A. monilatum. A substantial reduction of AOA abundance was subsequently observed during the A. monilatum bloom, followed by an increase in the post-bloom period of the early fall. Quantitative PCR (Q-PCR) of AOA and the two dinoflagellate species showed the same trends as the metabarcoding analyses. The reduction of AOA during the A. monilatum blooms might have resulted from dinoflagellate mixotrophy, as both M. polykrikoides and A. monilatum are mixotrophs. Our study indicates that AOA are a key player in carbon and nitrogen cycling in the lower YRE. Overall, results demonstrate that intense phytoplankton blooms exert a strong control on estuarine C cycling. The impact is especially pronounced during years of low to moderate freshwater discharge; while high discharge can result in particularly large spring blooms, it can also flush phytoplankton from the system before they can bloom. To date, this project has resulted in the training of six MS/PhD students, one postdoctoral fellow, and nine undergraduates. The project has resulted in 12 publications and 12 presentations at professional conferences to date. Data are archived at the Biological and Chemical Oceanography Data Management Office and in the NCBI-SRA database. Last Modified: 11/10/2023 Submitted by: MarkJBrush