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      Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida)

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          Abstract

          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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          Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.

          Nitrification, the microbial oxidation of ammonia to nitrite and nitrate, occurs in a wide variety of environments and plays a central role in the global nitrogen cycle. Catalyzed by the enzyme ammonia monooxygenase, the ability to oxidize ammonia was previously thought to be restricted to a few groups within the beta- and gamma-Proteobacteria. However, recent metagenomic studies have revealed the existence of unique ammonia monooxygenase alpha-subunit (amoA) genes derived from uncultivated, nonextremophilic Crenarchaeota. Here, we report molecular evidence for the widespread presence of ammonia-oxidizing archaea (AOA) in marine water columns and sediments. Using PCR primers designed to specifically target archaeal amoA, we find AOA to be pervasive in areas of the ocean that are critical for the global nitrogen cycle, including the base of the euphotic zone, suboxic water columns, and estuarine and coastal sediments. Diverse and distinct AOA communities are associated with each of these habitats, with little overlap between water columns and sediments. Within marine sediments, most AOA sequences are unique to individual sampling locations, whereas a small number of sequences are evidently cosmopolitan in distribution. Considering the abundance of nonextremophilic archaea in the ocean, our results suggest that AOA may play a significant, but previously unrecognized, role in the global nitrogen cycle.
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            Fundamentals of Microbial Community Resistance and Resilience

            Microbial communities are at the heart of all ecosystems, and yet microbial community behavior in disturbed environments remains difficult to measure and predict. Understanding the drivers of microbial community stability, including resistance (insensitivity to disturbance) and resilience (the rate of recovery after disturbance) is important for predicting community response to disturbance. Here, we provide an overview of the concepts of stability that are relevant for microbial communities. First, we highlight insights from ecology that are useful for defining and measuring stability. To determine whether general disturbance responses exist for microbial communities, we next examine representative studies from the literature that investigated community responses to press (long-term) and pulse (short-term) disturbances in a variety of habitats. Then we discuss the biological features of individual microorganisms, of microbial populations, and of microbial communities that may govern overall community stability. We conclude with thoughts about the unique insights that systems perspectives – informed by meta-omics data – may provide about microbial community stability.
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              Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil.

              Agricultural ecosystems annually receive approximately 25% of the global nitrogen input, much of which is oxidized at least once by ammonia-oxidizing prokaryotes to complete the nitrogen cycle. Recent discoveries have expanded the known ammonia-oxidizing prokaryotes from the domain Bacteria to Archaea. However, in the complex soil environment it remains unclear whether ammonia oxidation is exclusively or predominantly linked to Archaea as implied by their exceptionally high abundance. Here we show that Bacteria rather than Archaea functionally dominate ammonia oxidation in an agricultural soil, despite the fact that archaeal versus bacterial amoA genes are numerically more dominant. In soil microcosms, in which ammonia oxidation was stimulated by ammonium and inhibited by acetylene, activity change was paralleled by abundance change of bacterial but not of archaeal amoA gene copy numbers. Molecular fingerprinting of amoA genes also coupled ammonia oxidation activity with bacterial but not archaeal amoA gene patterns. DNA-stable isotope probing demonstrated CO(2) assimilation by Bacteria rather than Archaea. Our results indicate that Archaea were not important for ammonia oxidation in the agricultural soil tested.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                10 July 2020
                2020
                : 11
                : 1541
                Affiliations
                [1] 1School of Ocean Science and Engineering, The University of Southern Mississippi, Ocean Springs , MS, United States
                [2] 2Department of Earth and Environmental Sciences, Wright State University , Dayton, OH, United States
                [3] 3Section for Aquaculture, The North Sea Research Centre, DTU Aqua, Technical University of Denmark , Hirtshals, Denmark
                Author notes

                Edited by: Sebastian Lücker, Radboud University Nijmegen, Netherlands

                Reviewed by: Huiluo Cao, The University of Hong Kong, Hong Kong; Hidetoshi Urakawa, Florida Gulf Coast University, United States

                *Correspondence: Justyna J. Hampel, justyna.hampel@ 123456usm.edu

                This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2020.01541
                7366250
                f8385539-12df-4d00-a443-27d00bcfcb52
                Copyright © 2020 Hampel, McCarthy, Aalto and Newell.

                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.

                History
                : 21 April 2020
                : 12 June 2020
                Page count
                Figures: 8, Tables: 1, Equations: 1, References: 114, Pages: 17, Words: 0
                Funding
                Funded by: Florida Sea Grant, University of Florida 10.13039/100005789
                Award ID: PD-16-10
                Funded by: Eppley Foundation for Research 10.13039/100008887
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                aoa,aob,eutrophication,harmful algal blooms,hurricane,nitrification
                Microbiology & Virology
                aoa, aob, eutrophication, harmful algal blooms, hurricane, nitrification

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