Metabolic Diversity and Aero-Tolerance in Anammox Bacteria from Geochemically Distinct Aquifers

Mosley, Olivia E.; Gios, Emilie; Weaver, Louise; Close, Murray E.; Daughney, Christopher J.; Raaij, Rob van der; Martindale, Heather

doi:10.1128/msystems.01255-21

Cited by 22 publications

(28 citation statements)

References 117 publications

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“…Groundwater physicochemical parameters (Table S1 ) were measured as described by Mosley et al [ 30 ] (also see details on methods in Supplementary Materials ). Groundwater and sediment-enriched groundwater from the Canterbury meta-omics series were analyzed for heterotrophic cell counts using pour-plating assays.…”

Section: Methodsmentioning

confidence: 99%

“…Here we tested the prediction that Patescibacteria and DPANN are common to aquifer systems, and transcriptionally active across distinct redox conditions. Given compositional differences reported between planktonic and biofilm fractions of other groundwater prokaryotes [ 30 ], we also determined the compositional, genetic and transcriptional differences between planktonic and sediment-associated ultra-small community fractions. To assess the distribution, metabolic activity and environmental preferences of aquifer microbiomes, we collected 81 groundwater samples from 10 different aquifers spread over hundreds of kilometers [ 30 , 31 ].…”

Section: Introductionmentioning

confidence: 99%

“…Given compositional differences reported between planktonic and biofilm fractions of other groundwater prokaryotes [ 30 ], we also determined the compositional, genetic and transcriptional differences between planktonic and sediment-associated ultra-small community fractions. To assess the distribution, metabolic activity and environmental preferences of aquifer microbiomes, we collected 81 groundwater samples from 10 different aquifers spread over hundreds of kilometers [ 30 , 31 ]. This enabled us to determine associations between the ultra-small fraction and groundwater physicochemistry.…”

Section: Introductionmentioning

confidence: 99%

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Ultra-small bacteria and archaea exhibit genetic flexibility towards groundwater oxygen content, and adaptations for attached or planktonic lifestyles

Gios

Mosley

Weaver

et al. 2023

ISME Communications

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Aquifers are populated by highly diverse microbial communities, including unusually small bacteria and archaea. The recently described Patescibacteria (or Candidate Phyla Radiation) and DPANN radiation are characterized by ultra-small cell and genomes sizes, resulting in limited metabolic capacities and probable dependency on other organisms to survive. We applied a multi-omics approach to characterize the ultra-small microbial communities over a wide range of aquifer groundwater chemistries. Results expand the known global range of these unusual organisms, demonstrate the wide geographical range of over 11,000 subsurface-adapted Patescibacteria, Dependentiae and DPANN archaea, and indicate that prokaryotes with ultra-small genomes and minimalistic metabolism are a characteristic feature of the terrestrial subsurface. Community composition and metabolic activities were largely shaped by water oxygen content, while highly site-specific relative abundance profiles were driven by a combination of groundwater physicochemistries (pH, nitrate-N, dissolved organic carbon). We provide insights into the activity of ultra-small prokaryotes with evidence that they are major contributors to groundwater community transcriptional activity. Ultra-small prokaryotes exhibited genetic flexibility with respect to groundwater oxygen content, and transcriptionally distinct responses, including proportionally greater transcription invested into amino acid and lipid metabolism and signal transduction in oxic groundwater, along with differences in taxa transcriptionally active. Those associated with sediments differed from planktonic counterparts in species composition and transcriptional activity, and exhibited metabolic adaptations reflecting a surface-associated lifestyle. Finally, results showed that groups of phylogenetically diverse ultra-small organisms co-occurred strongly across sites, indicating shared preferences for groundwater conditions.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Ultra-small bacteria and archaea exhibit genetic flexibility towards groundwater oxygen content, and adaptations for attached or planktonic lifestyles

Gios

Mosley

Weaver

et al. 2023

ISME Communications

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“…Groundwater samples were collected from 8 wells from 2 sand/gravel aquifers in Canterbury, New Zealand, as described by (Mosley et al, 2022). Briefly, wells were purged (×3–5 bore volumes), then 3–90 L of groundwater was filtered per sample.…”

Section: Methodsmentioning

confidence: 99%

Genetic exchange shapes ultra-small Patescibacteria metabolic capacities in the terrestrial subsurface

Gios

Mosley

Takeuchi

2022

Preprint

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Bacterial genomes are highly dynamic entities, mostly due to the extent of horizontal gene transfer (HGT) occurring in these organisms. HGT is thought to be the main driver of genetic variation and adaptation to local environment in bacteria. However, little is known about the modalities of HGT within natural microbial communities, especially the implications of genetic exchange for streamlined microorganisms such as Patescibacteria (Candidate Phyla Radiation). We searched for evidence of genetic exchange in 125 Patescibacteria genomes recovered from aquifer environments and detected the presence of hundreds of genomic islands, individually transferred genes and prophage combined, with up to 29% of genome length attributed to HGT. Results show that most individual gene transfer events occurred between Patescibacteria, but donors were also phylogenetically diverse groundwater microorganisms. Using gene donor-recipient information, we identified one potential host (Omnitrophota) of the ultra-small bacteria, and confirmed this by matching relative abundance patterns across 16 groundwater samples. A wide variety of metabolic functions were introduced in Patescibacteria genomes by HGT including transcription, translation and DNA replication, recombination and repair. This study illustrates the evolutionarily dynamic nature of Patescibacteria genomes despite the constraints of streamlining, and that HGT in these organisms is also mediated via viral infection.

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“…While recent studies have suggested that anammox bacteria are most likely oxygen tolerant rather than strictly anaerobic 53,54 , the comparatively high abundance of anammox in the attached phase could also be due to anaerobic zones deeper in the biofilm. Further, transcriptional activity of anammox genes associated with Brocadia were found in aquifers with anoxic-to-oxic conditions suggesting anammox bacteria are able to contribute to nitrogen loss in a diverse range of oxygen environments 55 .…”

Section: Dissolved Oxygen Dependent Nitrification and Nitrogen Loss O...mentioning

confidence: 99%

Co-occurrence and cooperation between comammox and anammox bacteria in a full-scale attached growth municipal wastewater treatment process

Vilardi

Cotto

Bachmann

et al. 2022

Preprint

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Cooperation between comammox and anammox bacteria for nitrogen removal has been recently reported in laboratory-scale systems including synthetic community construct; however, there are no reports of full-scale municipal wastewater treatment systems with such cooperation. Here, we report intrinsic and extant kinetics as well as genome-resolved community characterization of a full-scale integrated fixed film activated sludge (IFAS) system where comammox and anammox bacteria co-occur and appear to drive nitrogen loss. Intrinsic batch kinetic assays indicated that majority of the aerobic ammonia oxidation was driven by comammox bacteria (1.75 ± 0.08 mg-N/g TS-h) in the attached growth phase with minimal contribution by ammonia oxidizing bacteria. Interestingly, a portion of total inorganic nitrogen (~8%) was consistently lost during these aerobic assays. Aerobic nitrite oxidation assays eliminated the possibility of denitrification as a cause of nitrogen loss, while anaerobic ammonia oxidation assays resulted in rates consistent with anammox stoichiometry. Full-scale experiments at different dissolved oxygen (DO = 2-6 mg/L) set points indicated persistent nitrogen loss that was partly sensitive to DO concentrations. Genome-resolved metagenomics confirmed high abundance (relative abundance 6.53 ± 0.34%) of two Brocadia-like anammox populations while comammox bacteria within the Ca. Nitrospira nitrosa cluster were lower in abundance (0.37% ± 0.03%) and Nitrosomonas-like ammonia oxidizers even lower (0.12% ± 0.02%). Collectively, our study reports for the first time the co-occurrence and co-operation of comammox and anammox bacteria in a full-scale municipal wastewater treatment system.

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Metabolic Diversity and Aero-Tolerance in Anammox Bacteria from Geochemically Distinct Aquifers

Cited by 22 publications

References 117 publications

Ultra-small bacteria and archaea exhibit genetic flexibility towards groundwater oxygen content, and adaptations for attached or planktonic lifestyles

Ultra-small bacteria and archaea exhibit genetic flexibility towards groundwater oxygen content, and adaptations for attached or planktonic lifestyles

Genetic exchange shapes ultra-small Patescibacteria metabolic capacities in the terrestrial subsurface

Co-occurrence and cooperation between comammox and anammox bacteria in a full-scale attached growth municipal wastewater treatment process

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