Metagenomic profiling of ammonia- and methane-oxidizing microorganisms in two sequential rapid sand filters

Poghosyan, Lianna; Koch, Hanna; Frank, J. Howard; Kessel, Maartje A. H. J. van; Cremers, Geert; Alen, Theo van; Jetten, Mike S. M.; Camp, Huub J. M. Op den; Lücker, Sebastian

doi:10.1016/j.watres.2020.116288

Cited by 61 publications

(32 citation statements)

References 96 publications

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“…Rapid sand filters (RSF), widely used to produce drinking water from surface-or groundwater, are useful model systems as they are characterized by stable conditions; active growth, primarily driven by the oxidation of ammonia, methane, and other inorganic compounds present at low concentration in the influent water; large populations (10 9 -10 10 cells/g); significant mixing; continuous but limited immigration from prokaryotes in the influent water; no dispersal between separate sand filters (resulting in allopatric populations); and relatively well defined coupling between chemical and biological processes (5)(6)(7)(8). In addition, the microbial communities inhabiting these systems, which are usually stable across time (9), have been broadly described, showing a general dominance of complete ammonia oxidizers (comammox) (6,10,11). These recently discovered microorganisms are expected to have a relatively simple ecology (due to their chemolithoautotrophic metabolism) (12), yet are poorly studied in terms of what drives their diversity, distribution and evolution.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary ecology of natural comammoxNitrospirapopulations

Palomo¹,

Dechesne²,

Cordero

et al. 2020

Preprint

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Microbial life on Earth commonly occurs in diverse and complex communities where species interact, and their genomic repertoires evolve over time. Our understanding of species interaction and evolution has increased during last decades, but most studies of evolutionary dynamics are based on single species in isolation or experimental systems composed of few interacting species. Here, we use the microbial ecosystem found in groundwater-fed sand filters as a model to avoid this limitation. In these systems, diverse microbial communities experience relatively stable conditions, and the coupling between chemical and biological processes is generally well defined. Metagenomic analysis of 12 sand filters revealed systematic co-occurrence of at least five comammox Nitrospira species, favoured by low ammonium concentrations. Nitrospira species showed intra-population sequence diversity, although possible clonal expansion was detected in few abundant local comammox populations. Nitrospira populations were separated by gene flow boundaries, suggesting natural and cohesive populations. They showed low homologous recombination and strong purifying selection, the latest process being especially strong in genes essential in energy metabolism. Positive selection was detected on genes related to resistance to foreign DNA and phages. Additionally, we analysed evolutionary processes in populations from different habitats. Interestingly, our results suggest that in comammox Nitrospira these processes are not an intrinsic feature but greatly vary depending on the habitat they inhabit. Compared to other habitats, groundwater fed sand filters impose strong purifying selection and low recombination. Together, this study improves understanding of interactions and evolution of species in the wild, and sheds light on the environmental dependency of evolutionary processes.

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Section: Introductionmentioning

confidence: 99%

Evolutionary ecology of natural comammoxNitrospirapopulations

Palomo¹,

Dechesne²,

Cordero

et al. 2020

Preprint

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“…However, most of these cases were unde ned. Similarly, Nitrospira was found to be abundant in oligotrophic water environments, such as drinking water systems (Oh et al 2017, Poghosyan et al 2020. In addition, it has been reported that Nitrospira is the only nitrite oxidising bacterium in SFs, with groundwater as the water source and accounts for 65% of all microorganisms (Vet et al 2009).…”

Section: Diversity and Composition Of Bacterial Communities In Sfsmentioning

confidence: 99%

Nitrogen-metabolising Microorganism Analysis in Rapid Sand Filters From Drinking Water Treatment Plant by Culturing and Metagenomics

Zhang

et al. 2021

Preprint

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Sand filter (SFs) are common treatment processes for nitrogen pollutants removal in drinking water treatment plants (DWTPs). However, the mechanisms on the nitrogen-cycling role of SFs are still unclear. In this study, 16S rRNA gene amplicon sequencing was used to characterise the diversity and composition of the bacterial community in SFs from DWTPs. Additionally, metagenomics approach was used to determine the functional microorganisms involved in nitrogen cycle in SFs. Our results showed that Proteobacteria, Acidobacteria, Nitrospirae, and Chloroflexi dominated in SFs. Subsequently, 85 high-quality metagenome-assembled genomes (MAGs) were retrieved from metagenome datasets of selected SFs involving nitrification, assimilatory nitrogen reduction, and denitrification processes. Read mapping to reference genomes of Nitrospira and the phylogenetic tree of the ammonia monooxygenase subunit A gene, amoA, suggested that Nitrospira is abundantly found in SFs. Furthermore, according to their genetic content, a nitrogen metabolic model in SFs was proposed using representative MAGs and pure culture isolates. Quantitative real-time polymerase chain reaction (PCR) showed that ammonia-oxidising bacteria (AOB) and archaea (AOA), and complete ammonia oxidisers (comammox) were ubiquitous in the SFs, with the abundance of comammox being higher than that of AOA and AOB. Moreover, we identified a bacterial strain with a high NO3-N removal rate as Pseudomonas sp., which could be applied in the bioremediation of micro-polluted drinking water sources. Our study provides insights into functional nitrogen-metabolising microbes in SFs of DWTPs.

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“…In contrast, comammox bacteria belonging to clade A1 were lower in abundance and did not demonstrate significant change over time in any amended microcosm. Though physiological differences between comammox bacteria clades/sub-clades have yet to be established, earlier studies of DWTP biofilters have observed higher abundances of clade B (15) or alternatively both clades found at the same DWTP but within separate rapid sand filters, where clade B was more abundant in the secondary filters receiving lower ammonia concentrations (34). In this study, the lack of clade A1 enrichment may also indicate distinct physiological niches within clades (i.e., subclade-level niche differentiation).…”

Section: Comammox Bacterial Abundance Increased Irrespective Of Nitrogen Source or Loading But May Compete With Nob Depending On Nitrogenmentioning

confidence: 99%

“…Beyond clade specific traits, identifying the potential environmental and physiological factors driving the coexistence of comammox bacteria with canonical nitrifiers is also important to better understand comammox bacteria role in complex nitrifying communities (21)(22)(23)(24)(25)(26)(27)(28)(29). Comammox bacteria have been detected along with their canonical nitrifying counterparts in wastewater treatment plants (18,25,(30)(31)(32), drinking water systems (6,9,15,33,34) and soils (22,28,35,36) at varying abundances over a wide range of ammonium concentrations. While there is currently no quantitative estimate of the contribution of comammox bacteria to nitrification compared to AOB and NOB, several studies have investigated comammox bacterial dynamics in the context of mixed nitrifying communities.…”

Section: Introductionmentioning

confidence: 99%

Comammox Nitrospira bacteria outnumber canonical nitrifiers irrespective of nitrogen source and availability

Vilardi

Cotto

Rivera

et al. 2021

Preprint

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Complete ammonia oxidizing bacteria coexist with canonical ammonia and nitrite oxidizing bacteria in a wide range of environments. Whether this coexistence is due to competitive or cooperative interactions between the three guilds, or a result of niche separation is not yet clear. Understanding the factors driving coexistence of nitrifying guilds is critical to effectively manage nitrification processes occurring in engineered and natural ecosystems. In this study, microcosms-based experiments were used to investigate the impact of electron donor mode (i.e., ammonia and urea) and loading on the population dynamics of nitrifying guilds in drinking water biofilter media. Shotgun sequencing of DNA from select time points followed by co-assembly and re-construction of metagenome assembled genomes (MAGs) revealed multiple clade A2 and one clade A1 comammox bacterial populations coexisted in the microcosms alongside Nitrosomonas-like ammonia oxidizers and Nitrospira-like nitrite oxidizer populations. Clade A2 comammox bacteria were likely the primary nitrifiers within the microcosms and increased in abundance over canonical ammonia and nitrite oxidizing bacteria irrespective of electron donor mode or nitrogen loading rates. This suggests that comammox bacteria will outnumber nitrifying communities sourced from oligotrophic environments irrespective of variable nitrogen regimes. Changes in comammox bacterial abundance were not correlated with either ammonia or nitrite oxidizing bacterial abundance in urea amended systems where metabolic reconstruction indicated potential cross feeding between ammonia and nitrite oxidizing bacteria. In contrast, comammox bacterial abundance demonstrated a negative correlation with that of nitrite oxidizers in ammonia amended systems. This suggests that potentially weaker synergistic relationships between ammonia and nitrite oxidizers might enable comammox bacteria to displace nitrite oxidizers from complex nitrifying communities.

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Metagenomic profiling of ammonia- and methane-oxidizing microorganisms in two sequential rapid sand filters

Cited by 61 publications

References 96 publications

Evolutionary ecology of natural comammoxNitrospirapopulations

Evolutionary ecology of natural comammoxNitrospirapopulations

Nitrogen-metabolising Microorganism Analysis in Rapid Sand Filters From Drinking Water Treatment Plant by Culturing and Metagenomics

Comammox Nitrospira bacteria outnumber canonical nitrifiers irrespective of nitrogen source and availability

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