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Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance.

ABSTRACT: BACKGROUND:Anaerobic ammonium oxidation (anammox) is a biological process employed to remove reactive nitrogen from wastewater. While a substantial body of literature describes the performance of anammox bioreactors under various operational conditions and perturbations, few studies have resolved the metabolic roles of their core microbial community members. RESULTS:Here, we used metagenomics to study the microbial community of a laboratory-scale anammox bioreactor from inoculation, through a performance destabilization event, to robust steady-state performance. Metabolic analyses revealed that nutrient acquisition from the environment is selected for in the anammox community. Dissimilatory nitrate reduction to ammonium (DNRA) was the primary nitrogen removal pathway that competed with anammox. Increased replication of bacteria capable of DNRA led to the out-competition of anammox bacteria, and the loss of the bioreactor's nitrogen removal capacity. These bacteria were highly associated with the anammox bacterium and considered part of the core microbial community. CONCLUSIONS:Our findings highlight the importance of metabolic interdependencies related to nitrogen- and carbon-cycling within anammox bioreactors and the potentially detrimental effects of bacteria that are otherwise considered core microbial community members.

SUBMITTER: Keren R

PROVIDER: S-EPMC6982389 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance.

Keren Ray R Lawrence Jennifer E JE Zhuang Weiqin W Jenkins David D Banfield Jillian F JF Alvarez-Cohen Lisa L Zhou Lijie L Yu Ke K

Microbiome 20200124 1

<h4>Background</h4>Anaerobic ammonium oxidation (anammox) is a biological process employed to remove reactive nitrogen from wastewater. While a substantial body of literature describes the performance of anammox bioreactors under various operational conditions and perturbations, few studies have resolved the metabolic roles of their core microbial community members.<h4>Results</h4>Here, we used metagenomics to study the microbial community of a laboratory-scale anammox bioreactor from inoculatio ...[more]

PMID: 31980038

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Project description:Anaerobic ammonia oxidizing bacteria (Anammox) are implemented in high-efficiency wastewater treatment systems operated in two general configurations; one-stage systems combine aerobic ammonia oxidizing bacteria (AOB) and Anammox within a single aerated reactor, whereas two-stage configurations separate these processes into discrete tanks. Within both configurations heterotrophic populations that perform denitrification or dissimilatory nitrate reduction to ammonia (DNRA) compete for carbon and nitrate or nitrite and can impact reactor performance because DNRA retains nitrogen in the system. Therefore, it is important to understand how selective pressures imposed by one-stage and two-stage reactor configurations impact the microbial community structure and associated nitrogen transforming functions. We performed 16S rRNA gene and metagenomic sequencing on different biomass fractions (granules, flocs, and suspended biomass) sampled from two facilities treating sludge dewatering centrate: a one-stage treatment facility (Chambers Creek, Tacoma, WA) and a two-stage system (Rotterdam, Netherlands). Similar microbial populations were identified across the different samples, but relative abundances differed between reactor configurations and biomass sources. Analysis of metagenome assembled genomes (MAGs) indicated different lifestyles for abundant heterotrophic populations. Acidobacteria, Bacteroidetes, and Chloroflexi MAGs had varying capacity for DNRA and denitrification. Acidobacteria MAGs possessed high numbers of glycosyl hydrolases and glycosyl transferases indicating a role in biomass degradation. Ignavibacteria and Phycosphaerae MAGs contributed to the greater relative abundance of DNRA associated nrf genes in the two-stage granules and contained genomic features suggesting a preference for an anoxic or microoxic niche. In the one-stage granules a MAG assigned to Burkholderiales accounted for much of the abundant denitrification genes and had genomic features, including the potential for autotrophic denitrification using reduced sulfur, that indicate an ability to adapt its physiology to varying redox conditions. Overall, the competition for carbon substrates between denitrifying and DNRA performing heterotrophs may be impacted by configuration specific selective pressures. In one-stage systems oxygen availability in the bulk liquid and the oxygen gradient within granules would provide a greater niche space for heterotrophic populations capable of utilizing both oxygen and nitrate or nitrite as terminal electron acceptors, compared to two-stage systems where a homogeneous anoxic environment would favor heterotrophic populations primarily adapted to anaerobic metabolism.

Project description:Environmental contamination with compounds containing oxyanions of chlorine, such as perchlorate or chlorate [(per)chlorate] or chlorine dioxide, has been a constantly growing problem over the last 100 years. Although the fact that microbes reduce these compounds has been recognized for more than 50 years, only six organisms which can obtain energy for growth by this metabolic process have been described. As part of a study to investigate the diversity and ubiquity of microorganisms involved in the microbial reduction of (per)chlorate, we enumerated the (per)chlorate-reducing bacteria (ClRB) in very diverse environments, including pristine and hydrocarbon-contaminated soils, aquatic sediments, paper mill waste sludges, and farm animal waste lagoons. In all of the environments tested, the acetate-oxidizing ClRB represented a significant population, whose size ranged from 2.31 x 10(3) to 2.4 x 10(6) cells per g of sample. In addition, we isolated 13 ClRB from these environments. All of these organisms could grow anaerobically by coupling complete oxidation of acetate to reduction of (per)chlorate. Chloride was the sole end product of this reductive metabolism. All of the isolates could also use oxygen as a sole electron acceptor, and most, but not all, could use nitrate. The alternative electron donors included simple volatile fatty acids, such as propionate, butyrate, or valerate, as well as simple organic acids, such as lactate or pyruvate. Oxidized-minus-reduced difference spectra of washed whole-cell suspensions of the isolates had absorbance maxima close to 425, 525, and 550 nm, which are characteristic of type c cytochromes. In addition, washed cell suspensions of all of the ClRB isolates could dismutate chlorite, an intermediate in the reductive metabolism of (per)chlorate, into chloride and molecular oxygen. Chlorite dismutation was a result of the activity of a single enzyme which in pure form had a specific activity of approximately 1,928 micromol of chlorite per mg of protein per min. Analyses of the 16S ribosomal DNA sequences of the organisms indicated that they all belonged to the alpha, beta, or gamma subclass of the Proteobacteria. Several were closely related to members of previously described genera that are not recognized for the ability to reduce (per)chlorate, such as the genera Pseudomonas and Azospirllum. However, many were not closely related to any previously described organism and represented new genera within the Proteobacteria. The results of this study significantly increase the limited number of microbial isolates that are known to be capable of dissimilatory (per)chlorate reduction and demonstrate the hitherto unrecognized phylogenetic diversity and ubiquity of the microorganisms that exhibit this type of metabolism.

Project description:Open-water unit process wetlands host a benthic diatomaceous and bacterial assemblage capable of nitrate removal from treated municipal wastewater with unexpected contributions from anammox processes. In exploring mechanistic drivers of anammox, 16S rRNA gene sequencing profiles of the biomat revealed significant microbial community shifts along the flow path and with depth. Notably, there was an increasing abundance of sulfate reducers (Desulfococcus and other Deltaproteobacteria) and anammox microorganisms (Brocadiaceae) with depth. Pore water profiles demonstrated that nitrate and sulfate concentrations exhibited a commensurate decrease with biomat depth accompanied by the accumulation of ammonium. Quantitative PCR targeting the anammox hydrazine synthase gene, hzsA, revealed a 3-fold increase in abundance with biomat depth as well as a 2-fold increase in the sulfate reductase gene, dsrA These microbial and geochemical trends were most pronounced in proximity to the influent region of the wetland where the biomat was thickest and influent nitrate concentrations were highest. While direct genetic queries for dissimilatory nitrate reduction to ammonium (DNRA) microorganisms proved unsuccessful, an increasing depth-dependent dominance of Gammaproteobacteria and diatoms that have previously been functionally linked to DNRA was observed. To further explore this potential, a series of microcosms containing field-derived biomat material confirmed the ability of the community to produce sulfide and reduce nitrate; however, significant ammonium production was observed only in the presence of hydrogen sulfide. Collectively, these results suggest that biogenic sulfide induces DNRA, which in turn can explain the requisite coproduction of ammonium and nitrite from nitrified effluent necessary to sustain the anammox community.IMPORTANCE This study aims to increase understanding of why and how anammox is occurring in an engineered wetland with limited exogenous contributions of ammonium and nitrite. In doing so, the study has implications for how geochemical parameters could potentially be leveraged to impact nutrient cycling and attenuation during the operation of treatment wetlands. The work also contributes to ongoing discussions about biogeochemical signatures surrounding anammox processes and enhances our understanding of the contributions of anammox processes in freshwater environments.

Project description:UNLABELLED:This study demonstrates the prevalence, phylogenetic diversity, and physiology of nitrate-reducing microorganisms capable of utilizing reduced humic acids (HA) as electron donors in agricultural soils. Most probable number (MPN) enumeration of agricultural soils revealed large populations (10(4) to 10(6) cells g(-1) soil) of microorganisms capable of reducing nitrate while oxidizing the reduced HA analog 2,6-anthrahydroquinone disulfonate (AH(2)DS) to its corresponding quinone. Nitrate-dependent HA-oxidizing organisms isolated from agricultural soils were phylogenetically diverse and included members of the Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria. Advective up-flow columns inoculated with corn plot soil and amended with reduced HA and nitrate supported both HA oxidation and enhanced nitrate reduction relative to no-donor or oxidized HA controls. The additional electron donating capacity of reduced HA could reasonably be attributed to the oxidation of reduced functional groups. Subsequent 16S rRNA gene-based high-density oligonucleotide microarray (PhyloChip) indicated that reduced HA columns supported the development of a bacterial community enriched with members of the Acidobacteria, Firmicutes, and Betaproteobacteria relative to the no-donor control and initial inoculum. This study identifies a previously unrecognized role for HA in stimulating denitrification processes in saturated soil systems. Furthermore, this study indicates that reduced humic acids impact soil geochemistry and the indigenous bacterial community composition. IMPORTANCE:This study identifies a new metabolic capacity in soil microbial communities that may be responsible for the mediation of significant nitrogen losses from soil systems. Nitrate-dependent humic acid (HA)-oxidizing organisms isolated from agricultural soils were phylogenetically diverse and included members of Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria. Advective up-flow columns inoculated with corn plot soil and amended with reduced HA and nitrate supported both HA oxidation and enhanced nitrate reduction relative to no-donor or oxidized HA controls. The additional electron donating capacity of reduced HA could reasonably be attributed to the oxidation of reduced functional groups.

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Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance.

Publications

Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance.

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