Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida)
Nitrification is an important biological link between oxidized and reduced forms of nitrogen (N). The efficiency of nitrification plays a key role in mitigating excess N in eutrophic systems, including those with cyanobacterial harmful algal blooms (cyanoHABs), since it can be closely coupled with d...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2020-07-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.01541/full |
| _version_ | 1818061358433828864 |
|---|---|
| author | Justyna J. Hampel Justyna J. Hampel Mark J. McCarthy Sanni L. Aalto Silvia E. Newell |
| author_facet | Justyna J. Hampel Justyna J. Hampel Mark J. McCarthy Sanni L. Aalto Silvia E. Newell |
| author_sort | Justyna J. Hampel |
| collection | DOAJ |
| description | Nitrification is an important biological link between oxidized and reduced forms of nitrogen (N). The efficiency of nitrification plays a key role in mitigating excess N in eutrophic systems, including those with cyanobacterial harmful algal blooms (cyanoHABs), since it can be closely coupled with denitrification and removal of excess N. Recent work suggests that competition for ammonium (NH4+) between ammonia oxidizers and cyanoHABs can help determine microbial community structure. Nitrification rates and ammonia-oxidizing archaeal (AOA) and bacterial (AOB) community composition and gene abundances were quantified in Lake Okeechobee and St. Lucie Estuary in southern Florida (United States). We sampled during cyanobacterial (Microcystis) blooms in July 2016 and August 2017 (2 weeks before Hurricane Irma) and 10 days after Hurricane Irma made landfall. Nitrification rates were low during cyanobacterial blooms in Lake Okeechobee and St. Lucie Estuary, while low bloom conditions in St. Lucie Estuary coincided with greater nitrification rates. Nitrification rates in the lake were correlated (R2 = 0.94; p = 0.006) with AOA amoA abundance. Following the hurricane, nitrification rates increased by an order of magnitude, suggesting that nitrifiers outcompeted cyanobacteria for NH4+ under turbid, poor light conditions. After Irma, AOA and AOB abundances increased in St. Lucie Estuary, while only AOB increased in Lake Okeechobee. AOA sequences clustered into three major lineages: Nitrosopumilales (NP), Nitrososphaerales (NS), and Nitrosotaleales (NT). Many of the lake OTUs placed within the uncultured and uncharacterized NS δ and NT β clades, suggesting that these taxa are ecologically important along this eutrophic, lacustrine to estuarine continuum. After the hurricane, the AOA community shifted toward dominance by freshwater clades in St. Lucie Estuary and terrestrial genera in Lake Okeechobee, likely due to high rainfall and subsequent increased turbidity and freshwater loading from the lake into the estuary. AOB community structure was not affected by the disturbance. AOA communities were consistently more diverse than AOB, despite fewer sequences recovered, including new, unclassified, eutrophic ecotypes, suggesting a wider ecological biogeography than the oligotrophic niche originally posited. These results and other recent reports contradict the early hypothesis that AOB dominate ammonia oxidation in high-nutrient or terrestrial-influenced systems. |
| first_indexed | 2024-12-10T13:47:03Z |
| format | Article |
| id | doaj.art-5c83c9246b064d9ebe8ae1962e14fba3 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-10T13:47:03Z |
| publishDate | 2020-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-5c83c9246b064d9ebe8ae1962e14fba32022-12-22T01:46:21ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-07-011110.3389/fmicb.2020.01541554278Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida)Justyna J. Hampel0Justyna J. Hampel1Mark J. McCarthy2Sanni L. Aalto3Silvia E. Newell4School of Ocean Science and Engineering, The University of Southern Mississippi, Ocean Springs, MS, United StatesDepartment of Earth and Environmental Sciences, Wright State University, Dayton, OH, United StatesDepartment of Earth and Environmental Sciences, Wright State University, Dayton, OH, United StatesSection for Aquaculture, The North Sea Research Centre, DTU Aqua, Technical University of Denmark, Hirtshals, DenmarkDepartment of Earth and Environmental Sciences, Wright State University, Dayton, OH, United StatesNitrification is an important biological link between oxidized and reduced forms of nitrogen (N). The efficiency of nitrification plays a key role in mitigating excess N in eutrophic systems, including those with cyanobacterial harmful algal blooms (cyanoHABs), since it can be closely coupled with denitrification and removal of excess N. Recent work suggests that competition for ammonium (NH4+) between ammonia oxidizers and cyanoHABs can help determine microbial community structure. Nitrification rates and ammonia-oxidizing archaeal (AOA) and bacterial (AOB) community composition and gene abundances were quantified in Lake Okeechobee and St. Lucie Estuary in southern Florida (United States). We sampled during cyanobacterial (Microcystis) blooms in July 2016 and August 2017 (2 weeks before Hurricane Irma) and 10 days after Hurricane Irma made landfall. Nitrification rates were low during cyanobacterial blooms in Lake Okeechobee and St. Lucie Estuary, while low bloom conditions in St. Lucie Estuary coincided with greater nitrification rates. Nitrification rates in the lake were correlated (R2 = 0.94; p = 0.006) with AOA amoA abundance. Following the hurricane, nitrification rates increased by an order of magnitude, suggesting that nitrifiers outcompeted cyanobacteria for NH4+ under turbid, poor light conditions. After Irma, AOA and AOB abundances increased in St. Lucie Estuary, while only AOB increased in Lake Okeechobee. AOA sequences clustered into three major lineages: Nitrosopumilales (NP), Nitrososphaerales (NS), and Nitrosotaleales (NT). Many of the lake OTUs placed within the uncultured and uncharacterized NS δ and NT β clades, suggesting that these taxa are ecologically important along this eutrophic, lacustrine to estuarine continuum. After the hurricane, the AOA community shifted toward dominance by freshwater clades in St. Lucie Estuary and terrestrial genera in Lake Okeechobee, likely due to high rainfall and subsequent increased turbidity and freshwater loading from the lake into the estuary. AOB community structure was not affected by the disturbance. AOA communities were consistently more diverse than AOB, despite fewer sequences recovered, including new, unclassified, eutrophic ecotypes, suggesting a wider ecological biogeography than the oligotrophic niche originally posited. These results and other recent reports contradict the early hypothesis that AOB dominate ammonia oxidation in high-nutrient or terrestrial-influenced systems.https://www.frontiersin.org/article/10.3389/fmicb.2020.01541/fullAOAAOBeutrophicationharmful algal bloomshurricanenitrification |
| spellingShingle | Justyna J. Hampel Justyna J. Hampel Mark J. McCarthy Sanni L. Aalto Silvia E. Newell Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida) Frontiers in Microbiology AOA AOB eutrophication harmful algal blooms hurricane nitrification |
| title | Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida) |
| title_full | Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida) |
| title_fullStr | Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida) |
| title_full_unstemmed | Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida) |
| title_short | Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida) |
| title_sort | hurricane disturbance stimulated nitrification and altered ammonia oxidizer community structure in lake okeechobee and st lucie estuary florida |
| topic | AOA AOB eutrophication harmful algal blooms hurricane nitrification |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2020.01541/full |
| work_keys_str_mv | AT justynajhampel hurricanedisturbancestimulatednitrificationandalteredammoniaoxidizercommunitystructureinlakeokeechobeeandstlucieestuaryflorida AT justynajhampel hurricanedisturbancestimulatednitrificationandalteredammoniaoxidizercommunitystructureinlakeokeechobeeandstlucieestuaryflorida AT markjmccarthy hurricanedisturbancestimulatednitrificationandalteredammoniaoxidizercommunitystructureinlakeokeechobeeandstlucieestuaryflorida AT sannilaalto hurricanedisturbancestimulatednitrificationandalteredammoniaoxidizercommunitystructureinlakeokeechobeeandstlucieestuaryflorida AT silviaenewell hurricanedisturbancestimulatednitrificationandalteredammoniaoxidizercommunitystructureinlakeokeechobeeandstlucieestuaryflorida |