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Responses of Active Ammonia Oxidizers and Nitrification Activity in Eutrophic Lake Sediments to Nitrogen and Temperature.

ABSTRACT: Ammonium concentrations and temperature drive the activities of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB), but their effects on these microbes in eutrophic freshwater sediments are unclear. In this study, surface sediments collected from areas of Taihu Lake (China) with different degrees of eutrophication were incubated under three levels of nitrogen input and temperature, and the autotrophic growth of ammonia oxidizers was assessed using 13C-labeled DNA-based stable-isotope probing (SIP), while communities were characterized using MiSeq sequencing and phylogenetic analysis of 16S rRNA genes. Nitrification rates in sediment microcosms were positively correlated with nitrogen inputs, but there was no marked association with temperature. Incubation of SIP microcosms indicated that AOA and AOB amoA genes were labeled by 13C at 20°C and 30°C in the slightly eutrophic sediment, and AOB amoA genes were labeled to a much greater extent than AOA amoA genes in the moderately eutrophic sediment after 56 days. Phylogenetic analysis of 13C-labeled 16S rRNA genes revealed that the active AOA were mainly affiliated with the Nitrosopumilus cluster, with the Nitrososphaera cluster dominating in the slightly eutrophic sediment at 30°C with low ammonium input (1?mM). Active AOB communities were more sensitive to nitrogen input and temperature than were AOA communities, and they were exclusively dominated by the Nitrosomonas cluster, which tended to be associated with Nitrosomonadaceae-like lineages. Nitrosomonas sp. strain Is79A3 tended to dominate the moderately eutrophic sediment at 10°C with greater ammonium input (2.86?mM). The relative abundance responses of the major active communities to nitrogen input and temperature gradients varied, indicating niche differentiation and differences in the physiological metabolism of ammonia oxidizers that are yet to be described.IMPORTANCE Both archaea and bacteria contribute to ammonia oxidation, which plays a central role in the global cycling of nitrogen and is important for reducing eutrophication in freshwater environments. The abundance and activities of ammonia-oxidizing archaea and bacteria in eutrophic limnic sediments vary with different ammonium concentrations or with seasonal shifts, and how the two factors affect nitrification activity, microbial roles, and active groups in different eutrophic sediments is unclear. The significance of our research is in identifying the archaeal and bacterial responses to anthropogenic activity and climate change, which will greatly enhance our understanding of the physiological metabolic differences of ammonia oxidizers.

SUBMITTER: Wu L

PROVIDER: S-EPMC6715836 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Responses of Active Ammonia Oxidizers and Nitrification Activity in Eutrophic Lake Sediments to Nitrogen and Temperature.

Wu Ling L Han Cheng C Zhu Guangwei G Zhong Wenhui W

Applied and environmental microbiology 20190829 18

Ammonium concentrations and temperature drive the activities of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB), but their effects on these microbes in eutrophic freshwater sediments are unclear. In this study, surface sediments collected from areas of Taihu Lake (China) with different degrees of eutrophication were incubated under three levels of nitrogen input and temperature, and the autotrophic growth of ammonia oxidizers was assessed using <sup>13</sup>C-labeled DNA-bas ...[more]

PMID: 31253684

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Project description:Rice paddy fields are characterized by regular flooding and nitrogen fertilization, but the functional importance of aerobic ammonia oxidizers and nitrite oxidizers under unique agricultural management is poorly understood. In this study, we report the differential contributions of ammonia-oxidizing archaea (AOA), bacteria (AOB) and nitrite-oxidizing bacteria (NOB) to nitrification in four paddy soils from different geographic regions (Zi-Yang (ZY), Jiang-Du (JD), Lei-Zhou (LZ) and Jia-Xing (JX)) that are representative of the rice ecosystems in China. In urea-amended microcosms, nitrification activity varied greatly with 11.9, 9.46, 3.03 and 1.43 μg NO3(-)-N g(-1) dry weight of soil per day in the ZY, JD, LZ and JX soils, respectively, over the course of a 56-day incubation period. Real-time quantitative PCR of amoA genes and pyrosequencing of 16S rRNA genes revealed significant increases in the AOA population to various extents, suggesting that their relative contributions to ammonia oxidation activity decreased from ZY to JD to LZ. The opposite trend was observed for AOB, and the JX soil stimulated only the AOB populations. DNA-based stable-isotope probing further demonstrated that active AOA numerically outcompeted their bacterial counterparts by 37.0-, 10.5- and 1.91-fold in (13)C-DNA from ZY, JD and LZ soils, respectively, whereas AOB, but not AOA, were labeled in the JX soil during active nitrification. NOB were labeled to a much greater extent than AOA and AOB, and the addition of acetylene completely abolished the assimilation of (13)CO2 by nitrifying populations. Phylogenetic analysis suggested that archaeal ammonia oxidation was predominantly catalyzed by soil fosmid 29i4-related AOA within the soil group 1.1b lineage. Nitrosospira cluster 3-like AOB performed most bacterial ammonia oxidation in the ZY, LZ and JX soils, whereas the majority of the (13)C-AOB in the JD soil was affiliated with the Nitrosomona communis lineage. The (13)C-NOB was overwhelmingly dominated by Nitrospira rather than Nitrobacter. A significant correlation was observed between the active AOA/AOB ratio and the soil oxidation capacity, implying a greater advantage of AOA over AOB under microaerophilic conditions. These results suggest the important roles of soil physiochemical properties in determining the activities of ammonia oxidizers and nitrite oxidizers.

Project description:Exploring nitrifiers in extreme environments is vital to expanding our understanding of nitrogen cycle and microbial diversity. This study presents that complete ammonia oxidation (comammox) Nitrospira, together with acidophilic ammonia-oxidizing archaea (AOA), dominate in the nitrifying guild in sediments of an acid mine lake (AML). The lake water was characterized by acidic pH below 5 with a high ammonium concentration of 175 mg-N/liter, which is rare on the earth. Nitrification was active in sediments with a maximum nitrate production potential of 70.5 μg-N/(g-dry weight [dw] day) for mixed sediments. Quantitative PCR assays determined that in AML sediments, comammox Nitrospira and AOA amoA genes had relative abundances of 52% and 41%, respectively, among the total amoA genes. Further assays with 16S rRNA and amoA gene amplicon sequencing and metagenomics confirmed their dominance and revealed that the comammox Nitrospira found in sediments belonged to comammox Nitrospira clade A.2. Metagenomic binning retrieved a metagenome-assembled genome (MAG) of the comammox Nitrospira from sediments (completeness = 96.76%), and phylogenomic analysis suggested that it was a novel comammox Nitrospira. Comparative genomic investigation revealed that this comammox Nitrospira contained diverse metal resistance genes and an acidophile-affiliated F-type ATPase. Moreover, it had a more diverse genomic characteristic on nitrogen metabolism than the AOA in sediments and canonical AOB did. The results suggest that comammox Nitrospira is a versatile nitrifier that can adapt to acidic environments even with high ammonium concentrations. IMPORTANCE Ammonia-oxidizing archaea (AOA) was previously considered the sole dominant ammonia oxidizer in acidic environments. This study, however, found that complete ammonia oxidation (comammox) Nitrospira was also a dominant ammonia oxidizer in the sediments of an acidic mine lake, which had an acidic pH < 5 and a high ammonium concentration of 175 mg-N/liter. In combination with average nucleotide identity analysis, phylogenomic analysis suggested it is a novel strain of comammox Nitrospira. Moreover, the adaption of comammox Nitrospira to the acidic lake had been comprehensively investigated based on genome-centric metagenomic approaches. The outcomes of this study significantly expand our understanding of the diversity and adaptability of ammonia oxidizers in the acidic environments.

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Responses of Active Ammonia Oxidizers and Nitrification Activity in Eutrophic Lake Sediments to Nitrogen and Temperature.

Publications

Responses of Active Ammonia Oxidizers and Nitrification Activity in Eutrophic Lake Sediments to Nitrogen and Temperature.

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