Archaeal nitrification is constrained by copper complexation with organic matter in municipal wastewater treatment plants

Gwak, Joo-Han; Jung, Man‐Young; Hong, Heeji; Kim, Jong-Geol; Quan, Zhe‐Xue; Reinfelder, John R.; Spasov, Emilie; Neufeld, Josh D.; Wagner, Michael; Rhee, Sung‐Keun

doi:10.1038/s41396-019-0538-1

Cited by 70 publications

(37 citation statements)

References 63 publications

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“…This could be explained by the accumulation of organic compounds under drought, some of which were shown to inhibit Nitrosotalea activity and growth in pure cultures [ 92 ] compared with other AOA such as N. viennensis and N. gargensis [ 88 , 93 ]. Furthermore, inhibition by organic compounds has been shown to be stronger in AOA than in AOB, although it varies between AOA strains [ 94 , 95 ].…”

Section: Discussionmentioning

confidence: 99%

Composition and activity of nitrifier communities in soil are unresponsive to elevated temperature and CO2, but strongly affected by drought

et al. 2020

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Nitrification is a fundamental process in terrestrial nitrogen cycling. However, detailed information on how climate change affects the structure of nitrifier communities is lacking, specifically from experiments in which multiple climate change factors are manipulated simultaneously. Consequently, our ability to predict how soil nitrogen (N) cycling will change in a future climate is limited. We conducted a field experiment in a managed grassland and simultaneously tested the effects of elevated atmospheric CO2, temperature, and drought on the abundance of active ammonia-oxidizing bacteria (AOB) and archaea (AOA), comammox (CMX) Nitrospira, and nitrite-oxidizing bacteria (NOB), and on gross mineralization and nitrification rates. We found that N transformation processes, as well as gene and transcript abundances, and nitrifier community composition were remarkably resistant to individual and interactive effects of elevated CO2 and temperature. During drought however, process rates were increased or at least maintained. At the same time, the abundance of active AOB increased probably due to higher NH4+ availability. Both, AOA and comammox Nitrospira decreased in response to drought and the active community composition of AOA and NOB was also significantly affected. In summary, our findings suggest that warming and elevated CO2 have only minor effects on nitrifier communities and soil biogeochemical variables in managed grasslands, whereas drought favors AOB and increases nitrification rates. This highlights the overriding importance of drought as a global change driver impacting on soil microbial community structure and its consequences for N cycling.

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Section: Discussionmentioning

confidence: 99%

Composition and activity of nitrifier communities in soil are unresponsive to elevated temperature and CO2, but strongly affected by drought

et al. 2020

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“…In terrestrial environments, its bioavailability is influenced primarily by organic matter content and pH [ 13 ]. Recently, Gwak et al [ 14 ] showed that mixtures of organic compounds like yeast extract depleted Cu in culture experiments with AOA and AOB. However, only AOA growth was inhibited by reduced Cu bioavailability.…”

Section: Introductionmentioning

confidence: 99%

Genome wide transcriptomic analysis of the soil ammonia oxidizing archaeon Nitrososphaera viennensis upon exposure to copper limitation

et al. 2020

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Ammonia-oxidizing archaea (AOA) are widespread in nature and are involved in nitrification, an essential process in the global nitrogen cycle. The enzymes for ammonia oxidation and electron transport rely heavily on copper (Cu), which can be limited in nature. In this study the model soil archaeon Nitrososphaera viennensis was investigated via transcriptomic analysis to gain insight regarding possible Cu uptake mechanisms and compensation strategies when Cu becomes limiting. Upon Cu limitation, N. viennensis exhibited impaired nitrite production and thus growth, which was paralleled by downregulation of ammonia oxidation, electron transport, carbon fixation, nucleotide, and lipid biosynthesis pathway genes. Under Cu-limitation, 1547 out of 3180 detected genes were differentially expressed, with 784 genes upregulated and 763 downregulated. The most highly upregulated genes encoded proteins with a possible role in Cu binding and uptake, such as the Cu chelator and transporter CopC/D, disulfide bond oxidoreductase D (dsbD), and multicopper oxidases. While this response differs from the marine strain Nitrosopumilus maritimus, conserved sequence motifs in some of the Cu-responsive genes suggest conserved transcriptional regulation in terrestrial AOA. This study provides possible gene regulation and energy conservation mechanisms linked to Cu bioavailability and presents the first model for Cu uptake by a soil AOA.

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“…Due to the presence of anaerobic and anoxic phases, DPRS exhibits greater nitrification capacity and phosphorus removal performance than activated sludge [ 6 ]. But heavy metals can cause dysfunctions of proteins and inhibit microbial activities such as nitrification [ 7 , 8 ] and eventually attenuate the treatment efficiency [ 5 , 9 ]. Thus, a better understanding of the heavy metal-resistance strategies adopted by DPRS microbiomes might ultimately improve their robustness for nutrient removal.…”

Section: Introductionmentioning

confidence: 99%

Revealing taxon-specific heavy metal-resistance mechanisms in denitrifying phosphorus removal sludge using genome-centric metaproteomics

Lin

Wang

et al. 2021

Microbiome

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Background Denitrifying phosphorus removal sludge (DPRS) is widely adopted for nitrogen and phosphorus removal in wastewater treatment but faces threats from heavy metals. However, a lack of understanding of the taxon-specific heavy metal-resistance mechanisms hinders the targeted optimization of DPRS’s robustness in nutrient removal. Results We obtained 403 high- or medium-quality metagenome-assembled genomes from DPRS treated by elevating cadmium, nickel, and chromium pressure. Then, the proteomic responses of individual taxa under heavy metal pressures were characterized, with an emphasis on functions involving heavy metal resistance and maintenance of nutrient metabolism. When oxygen availability was constrained by high-concentration heavy metals, comammox Nitrospira overproduced highly oxygen-affinitive hemoglobin and electron-transporting cytochrome c-like proteins, underpinning its ability to enhance oxygen acquisition and utilization. In contrast, Nitrosomonas overexpressed ammonia monooxygenase and nitrite reductase to facilitate the partial nitrification and denitrification process for maintaining nitrogen removal. Comparisons between phosphorus-accumulating organisms (PAOs) demonstrated different heavy metal-resistance mechanisms adopted by Dechloromonas and Candidatus Accumulibacter, despite their high genomic similarities. In particular, Dechloromonas outcompeted the canonical PAO Candidatus Accumulibacter in synthesizing polyphosphate, a potential public good for heavy metal detoxification. The superiority of Dechloromonas in energy utilization, radical elimination, and damaged cell component repair also contributed to its dominance under heavy metal pressures. Moreover, the enrichment analysis revealed that functions involved in extracellular polymeric substance formation, siderophore activity, and heavy metal efflux were significantly overexpressed due to the related activities of specific taxa. Conclusions Our study demonstrates that heavy metal-resistance mechanisms within a multipartite community are highly heterogeneous between different taxa. These findings provide a fundamental understanding of how the heterogeneity of individual microorganisms contributes to the metabolic versatility and robustness of microbiomes inhabiting dynamic environments, which is vital for manipulating the adaptation of microbial assemblages under adverse environmental stimuli.

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Archaeal nitrification is constrained by copper complexation with organic matter in municipal wastewater treatment plants

Cited by 70 publications

References 63 publications

Composition and activity of nitrifier communities in soil are unresponsive to elevated temperature and CO2, but strongly affected by drought

Composition and activity of nitrifier communities in soil are unresponsive to elevated temperature and CO2, but strongly affected by drought

Genome wide transcriptomic analysis of the soil ammonia oxidizing archaeon Nitrososphaera viennensis upon exposure to copper limitation

Revealing taxon-specific heavy metal-resistance mechanisms in denitrifying phosphorus removal sludge using genome-centric metaproteomics

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