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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...

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Autores principales: Hampel, Justyna J., McCarthy, Mark J., Aalto, Sanni L., Newell, Silvia E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7366250/
https://www.ncbi.nlm.nih.gov/pubmed/32754132
http://dx.doi.org/10.3389/fmicb.2020.01541
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author Hampel, Justyna J.
McCarthy, Mark J.
Aalto, Sanni L.
Newell, Silvia E.
author_facet Hampel, Justyna J.
McCarthy, Mark J.
Aalto, Sanni L.
Newell, Silvia E.
author_sort Hampel, Justyna J.
collection PubMed
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 (NH(4)(+)) 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 (R(2) = 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 NH(4)(+) 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.
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spelling pubmed-73662502020-08-03 Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida) Hampel, Justyna J. McCarthy, Mark J. Aalto, Sanni L. Newell, Silvia E. Front Microbiol Microbiology 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 (NH(4)(+)) 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 (R(2) = 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 NH(4)(+) 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. Frontiers Media S.A. 2020-07-10 /pmc/articles/PMC7366250/ /pubmed/32754132 http://dx.doi.org/10.3389/fmicb.2020.01541 Text en Copyright © 2020 Hampel, McCarthy, Aalto and Newell. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Hampel, Justyna J.
McCarthy, Mark J.
Aalto, Sanni L.
Newell, Silvia E.
Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida)
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 Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7366250/
https://www.ncbi.nlm.nih.gov/pubmed/32754132
http://dx.doi.org/10.3389/fmicb.2020.01541
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