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Ammonium recycling supports toxic Planktothrix blooms in Sandusky Bay, Lake Erie: Evidence from stable isotope and metatranscriptome data.
Harmful Algae. 2019 01; 81:42-52.HA

Abstract

Sandusky Bay, Lake Erie, receives high nutrient loadings (nitrogen and phosphorus) from the Sandusky River, which drains an agricultural watershed. Eutrophication and cyanobacterial harmful algal blooms (cyanoHABs) persist throughout summer. Planktothrix agardhii is the dominant bloom-forming species and the main producer of microcystins in Sandusky Bay. Non-N2 fixing cyanobacteria, such as Planktothrix and Microcystis, thrive on chemically reduced forms of nitrogen, such as ammonium (NH4+) and urea. Ammonium regeneration and potential uptake rates and total microbial community demand for NH4+ were quantified in Sandusky Bay. Potential NH4+ uptake rates in the light increased from June to August at all stations. Dark uptake rates also increased seasonally and, by the end of August, were on par with light uptake rates. Regeneration rates followed a similar pattern and were significantly higher in August than June. Ammonium uptake kinetics during a Planktothrix-dominated bloom in Sandusky Bay and a Microcystis-dominated bloom in Maumee Bay were also compared. The highest half saturation constant (Km) in Sandusky Bay was measured in June and decreased throughout the season. In contrast, Km values in Maumee Bay were lowest at the beginning of summer and increased in October. A significant increase in Vmax in Sandusky Bay was observed between July and the end of August, reflective of intense competition for depleted NH4+. Metatranscriptome results from Sandusky Bay show a shift from cyanophycin synthetase (luxury NH4+ uptake; cphA1) expression in early summer to cyanophycinase (intracellular N mobilization; cphB/cphA2) expression in August, supporting the interpretation that the microbial community is nitrogen-starved in late summer. Combined, our results show that, in late summer, when nitrogen concentrations are low, cyanoHABs in Sandusky Bay rely on regenerated NH4+ to support growth and toxin production. Increased dark NH4+ uptake late in summer suggests an important heterotrophic contribution to NH4+ depletion in the phycosphere. Kinetic experiments in the two bays suggest a competitive advantage for Planktothrix over Microcystis in Sandusky Bay due to its higher affinity for NH4+ at low concentrations.

Authors+Show Affiliations

Department of Earth & Environmental Sciences, Wright State University, Dayton, OH, United States. Electronic address: hampel.4@wright.edu.Department of Earth & Environmental Sciences, Wright State University, Dayton, OH, United States.Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, United States.Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, United States.Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, United States.Department of Earth & Environmental Sciences, Wright State University, Dayton, OH, United States.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

30638497

Citation

Hampel, Justyna J., et al. "Ammonium Recycling Supports Toxic Planktothrix Blooms in Sandusky Bay, Lake Erie: Evidence From Stable Isotope and Metatranscriptome Data." Harmful Algae, vol. 81, 2019, pp. 42-52.
Hampel JJ, McCarthy MJ, Neudeck M, et al. Ammonium recycling supports toxic Planktothrix blooms in Sandusky Bay, Lake Erie: Evidence from stable isotope and metatranscriptome data. Harmful Algae. 2019;81:42-52.
Hampel, J. J., McCarthy, M. J., Neudeck, M., Bullerjahn, G. S., McKay, R. M. L., & Newell, S. E. (2019). Ammonium recycling supports toxic Planktothrix blooms in Sandusky Bay, Lake Erie: Evidence from stable isotope and metatranscriptome data. Harmful Algae, 81, 42-52. https://doi.org/10.1016/j.hal.2018.11.011
Hampel JJ, et al. Ammonium Recycling Supports Toxic Planktothrix Blooms in Sandusky Bay, Lake Erie: Evidence From Stable Isotope and Metatranscriptome Data. Harmful Algae. 2019;81:42-52. PubMed PMID: 30638497.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Ammonium recycling supports toxic Planktothrix blooms in Sandusky Bay, Lake Erie: Evidence from stable isotope and metatranscriptome data. AU - Hampel,Justyna J, AU - McCarthy,Mark J, AU - Neudeck,Michelle, AU - Bullerjahn,George S, AU - McKay,Robert Michael L, AU - Newell,Silvia E, Y1 - 2018/12/01/ PY - 2018/05/10/received PY - 2018/08/10/revised PY - 2018/11/16/accepted PY - 2019/1/15/entrez PY - 2019/1/15/pubmed PY - 2020/2/23/medline KW - Cyanobacteria KW - Lake Erie KW - Nitrogen KW - Nutrient management KW - Planktothrix KW - Sandusky Bay SP - 42 EP - 52 JF - Harmful algae JO - Harmful Algae VL - 81 N2 - Sandusky Bay, Lake Erie, receives high nutrient loadings (nitrogen and phosphorus) from the Sandusky River, which drains an agricultural watershed. Eutrophication and cyanobacterial harmful algal blooms (cyanoHABs) persist throughout summer. Planktothrix agardhii is the dominant bloom-forming species and the main producer of microcystins in Sandusky Bay. Non-N2 fixing cyanobacteria, such as Planktothrix and Microcystis, thrive on chemically reduced forms of nitrogen, such as ammonium (NH4+) and urea. Ammonium regeneration and potential uptake rates and total microbial community demand for NH4+ were quantified in Sandusky Bay. Potential NH4+ uptake rates in the light increased from June to August at all stations. Dark uptake rates also increased seasonally and, by the end of August, were on par with light uptake rates. Regeneration rates followed a similar pattern and were significantly higher in August than June. Ammonium uptake kinetics during a Planktothrix-dominated bloom in Sandusky Bay and a Microcystis-dominated bloom in Maumee Bay were also compared. The highest half saturation constant (Km) in Sandusky Bay was measured in June and decreased throughout the season. In contrast, Km values in Maumee Bay were lowest at the beginning of summer and increased in October. A significant increase in Vmax in Sandusky Bay was observed between July and the end of August, reflective of intense competition for depleted NH4+. Metatranscriptome results from Sandusky Bay show a shift from cyanophycin synthetase (luxury NH4+ uptake; cphA1) expression in early summer to cyanophycinase (intracellular N mobilization; cphB/cphA2) expression in August, supporting the interpretation that the microbial community is nitrogen-starved in late summer. Combined, our results show that, in late summer, when nitrogen concentrations are low, cyanoHABs in Sandusky Bay rely on regenerated NH4+ to support growth and toxin production. Increased dark NH4+ uptake late in summer suggests an important heterotrophic contribution to NH4+ depletion in the phycosphere. Kinetic experiments in the two bays suggest a competitive advantage for Planktothrix over Microcystis in Sandusky Bay due to its higher affinity for NH4+ at low concentrations. SN - 1878-1470 UR - https://www.unboundmedicine.com/medline/citation/30638497/Ammonium_recycling_supports_toxic_Planktothrix_blooms_in_Sandusky_Bay_Lake_Erie:_Evidence_from_stable_isotope_and_metatranscriptome_data_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1568-9883(18)30172-0 DB - PRIME DP - Unbound Medicine ER -