A single <i>Thaumarchaeon</i> drives nitrification in deep oligotrophic Lake Constance

Herber, Janina; Klotz, F.; Frommeyer, Benjamin; Weis, Severin; Straile, Dietmar; Kolar, Allison; Sikorski, Johannes; Egert, Markus; Dannenmann, Michael; Pester, Michael

doi:10.1111/1462-2920.14840

Cited by 39 publications

(51 citation statements)

References 103 publications

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“…However, the discovery of complete ammonia-oxidizing (comammox) bacteria, which possess both AMO and NXR and can oxidize ammonia to nitrate via nitrite, refuted the century-old paradigm and redefined key processes in the biogeochemical nitrogen cycle (3,4). All known comammox bacteria belong to the genus Nitrospira (3)(4)(5)(6)(7)(8), which was previously regarded as the dominant nitrite oxidizer in many artificial (e.g., wastewater treatment plants and drinking water systems) and natural (e.g., soil and freshwater) environments (9)(10)(11)(12)(13)(14)(15).…”

mentioning

confidence: 99%

Use of Newly Designed Primers for Quantification of Complete Ammonia-Oxidizing (Comammox) Bacterial Clades and Strict Nitrite Oxidizers in the Genus Nitrospira

Jiang

Wang

Zhu

et al. 2020

Appl Environ Microbiol

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Complete ammonia oxidizing (comammox) bacteria play key roles in environmental nitrogen cycling and all belong to the genus Nitrospira, which was originally believed to include only strict nitrite-oxidizing bacteria (sNOB). Thus, differential estimation of sNOB abundance from comammox Nitrospira has become problematic since both contain nitrite oxidoreductase genes that serve as common targets for sNOB detection. Herein, we developed novel comammox Nitrospira clades A- and B-specific primer sets targeting the α-subunit of ammonia monooxygenase gene (amoA) and a sNOB-specific primer set targeting cyanase gene (cynS) for quantitative PCR (qPCR). The high coverage and specificity of these primers had been checked by metagenome and metatranscriptome datasets. Efficient and specific amplification with these primers were demonstrated using various environmental samples. Using the newly designed primers, we successfully estimated the abundances of comammox Nitrospira and sNOB in samples from two chloramination-treated drinking water systems and found that, in most samples, comammox Nitrospira clade A was the dominant Nitrospira, and also served as the primary ammonia oxidizer. Compared with other ammonia oxidizers, comammox Nitrospira took advantage in process water samples in these two drinking water systems. We also demonstrated sNOB can be readily misrepresented with the previous method, calculated by subtracting the comammox abundance from the total Nitrospira, especially when the comammox Nitrospira proportion is relatively high. The new primer sets were successfully applied for the quantification of comammox Nitrospira and sNOB, which may prove useful in understanding the roles of Nitrospira in nitrification in various ecosystems. Importance Nitrospira is a dominant nitrite-oxidizing bacteria in many artificial and natural environments. The discovery of complete ammonia oxidizers in Nitrospira prevents the use of previously identified primers targeting Nitrospira 16S rRNA gene or nitrite oxidoreductase (nxr) gene for differential determination of strict nitrite-oxidizing bacteria in Nitrospira (sNOB) and comammox Nitrospira. We designed three novel primer sets that enabled quantification of comammox Nitrospira clades A and B and sNOB with high coverage, specificity, and accuracy in various environments. With designed primer sets, sNOB and comammox Nitrospira were differentially estimated in drinking water systems, and we found that comammox clade A was overcome sNOB and other ammonia oxidizers in process water samples. Accurate quantification of comammox Nitrospira and sNOB using the newly designed primers will provide essential information for evaluating the contribution of Nitrospira to nitrification in various ecosystems.

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confidence: 99%

Use of Newly Designed Primers for Quantification of Complete Ammonia-Oxidizing (Comammox) Bacterial Clades and Strict Nitrite Oxidizers in the Genus Nitrospira

Jiang

Wang

Zhu

et al. 2020

Appl Environ Microbiol

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“…This subgroup includes the family Vicinamibacteraceae, known for a wide range of substrate preferences including recalcitrant C (e.g., chitin) and labile C [82,84], thus being functionally versatile and important to maintain functions in a given soil. Gaiellaceae [85] and Nitrospiraceae [86] were also characterized by oligotrophic lifestyles, yet the role of these families in litter decomposition is largely unknown. However, Actinobacteria were recently described as generalists in litter decomposition and contributed to nutrient mobilization [87].…”

Section: Oligotrophic Bacteria and Litter Decompositionmentioning

confidence: 99%

Soil Bacterial Diversity Is Positively Correlated with Decomposition Rates during Early Phases of Maize Litter Decomposition

et al. 2021

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This study aimed to investigate the effects of different levels of soil- and plant-associated bacterial diversity on the rates of litter decomposition, and bacterial community dynamics during its early phases. We performed an incubation experiment where soil bacterial diversity (but not abundance) was manipulated by autoclaving and reinoculation. Natural or autoclaved maize leaves were applied to the soils and incubated for 6 weeks. Bacterial diversity was assessed before and during litter decomposition using 16S rRNA gene metabarcoding. We found a positive correlation between litter decomposition rates and soil bacterial diversity. The soil with the highest bacterial diversity was dominated by oligotrophic bacteria including Acidobacteria, Nitrospiraceae, and Gaiellaceae, and its community composition did not change during the incubation. In the less diverse soils, those taxa were absent but were replaced by copiotrophic bacteria, such as Caulobacteraceae and Beijerinckiaceae, until the end of the incubation period. SourceTracker analysis revealed that litter-associated bacteria, such as Beijerinckiaceae, only became part of the bacterial communities in the less diverse soils. This suggests a pivotal role of oligotrophic bacteria during the early phases of litter decomposition and the predominance of copiotrophic bacteria at low diversity.

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“…Although the iRep algorithm was recently questioned to work with population genomes integrating over many co-occurring but heterogeneous close relatives 29 , it performs well for uniform population genomes such as pure cultures 28,30,31 . We consider the extremely low and highly skewed AOA diversity in Lake Constance 16 to be rather representative of the latter case. Phylogenomic analysis placed AOA-LC4 within a freshwater/brackish water-associated clade of the Nitrosopumilaceae, which was distinct from marine representatives (Supplementary Fig.…”

Section: A Freshwater-specific Aoa Species Dominates the Nitrifier Communitymentioning

confidence: 99%

Quantification of archaea-driven freshwater nitrification: from single cell to ecosystem level

Klotz

Kitzinger

Ngugi

et al. 2021

Preprint

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Deep oligotrophic lakes sustain large archaeal populations of the class Nitrososphaeria in their hypolimnion. They are thought to be the key ammonia oxidizers in these freshwater systems and as such responsible for the rate-limiting step in nitrification. However, the impact that planktonic Nitrososphaeria have on N cycling in lakes is severely understudied and yet to be quantified. Here, we followed this archaeal population in one of Central Europe's largest lakes, Lake Constance, over two consecutive years using metagenomics and metatranscriptomics combined with stable isotope-based activity measurements. A single, highly abundant and transcriptionally active freshwater ecotype of Nitrososphaeria dominated the nitrifying community. Phylogenomic analysis of its metagenome-assembled genome showed that this ecotype represents a new lacustrine Nitrosopumilus species. Stable isotope probing revealed that Nitrososphaeria incorporated significantly more 15N-labeled ammonium than most other microorganisms at near-natural conditions and oxidized ammonia at an average rate of 0.22 ± 0.11 fmol cell-1 d-1. This translates to 1.9 gigagram of ammonia oxidized per year, corresponding to 12% of the N-biomass produced annually by photosynthetic organisms in Lake Constance. Here, we show that ammonia-oxidizing archaea play an equally important role in the nitrogen cycle of deep oligotrophic lakes as their counterparts in marine ecosystems.

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A single Thaumarchaeon drives nitrification in deep oligotrophic Lake Constance

Cited by 39 publications

References 103 publications

Use of Newly Designed Primers for Quantification of Complete Ammonia-Oxidizing (Comammox) Bacterial Clades and Strict Nitrite Oxidizers in the Genus Nitrospira

Use of Newly Designed Primers for Quantification of Complete Ammonia-Oxidizing (Comammox) Bacterial Clades and Strict Nitrite Oxidizers in the Genus Nitrospira

Soil Bacterial Diversity Is Positively Correlated with Decomposition Rates during Early Phases of Maize Litter Decomposition

Quantification of archaea-driven freshwater nitrification: from single cell to ecosystem level

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