Metabolic network analysis reveals microbial community interactions in anammox granules

Microbial communities mediating anaerobic ammonium oxidation (anammox) represent one of the most energy-efficient environmental biotechnologies for nitrogen removal from wastewater. However, little is known about the functional role heterotrophic bacteria play in anammox granules. Here, we use genome-centric metagenomics to recover 17 draft genomes of anammox and heterotrophic bacteria from a laboratory-scale anammox bioreactor. We combine metabolic network reconstruction with metatranscriptomics to examine the gene expression of anammox and heterotrophic bacteria and to identify their potential interactions. We find that Chlorobi-affiliated bacteria may be highly active protein degraders, catabolizing extracellular peptides while recycling nitrate to nitrite. Other heterotrophs may also contribute to scavenging of detritus and peptides produced by anammox bacteria, and potentially use alternative electron donors, such as H2, acetate and formate. Our findings improve the understanding of metabolic activities and interactions between anammox and heterotrophic bacteria and offer the first transcriptional insights on ecosystem function in anammox granules. The use of anammox microbiomes to treat wastewater is an escalating biotechnology, yet the functional role heterotrophic bacteria play in these systems remains poorly understood. Here, Lawsonet al. use metagenomics and metatranscriptomics to reveal that heterotrophs degrade free peptides, while recycling nitrate to nitrite.

• Publication year

  2017

• Venue

  Nature Communications

• Publication date

  2017-05-31

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1038/ncomms15416PMID 28561030PMCID 5460018
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Pathway Tools version 19.0 update: software for pathway/genome informatics and systems biology

  2016cited by this paper
• Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates

  2016cited by this paper
• Assessment of Heterotrophic Growth Supported by Soluble Microbial Products in Anammox Biofilm using Multidimensional Modeling

  2016cited by this paper
• Microbial interactions lead to rapid micro-scale successions on model marine particles

  2016cited by this paper
• Genome-based microbial ecology of anammox granules in a full-scale wastewater treatment system

  2016influential reference
• Source identification of nitrous oxide emission pathways from a single-stage nitritation-anammox granular reactor.

  2016cited by this paper
• Hydroxylamine-dependent anaerobic ammonium oxidation (anammox) by "Candidatus Brocadia sinica".

  2016cited by this paper
• Rare taxa have potential to make metabolic contributions in enhanced biological phosphorus removal ecosystems.

  2015cited by this paper
• Role of extracellular polymeric substance in determining the high aggregation ability of anammox sludge.

  2015cited by this paper
• Draft Genome Sequence of an Anaerobic Ammonium-Oxidizing Bacterium, “Candidatus Brocadia sinica”

  2015cited by this paper
• The effect of inorganic carbon on microbial interactions in a biofilm nitritation-anammox process.

  2015cited by this paper
• MetaPathways v2.5: quantitative functional, taxonomic and usability improvements

  2015cited by this paper
• Microbial community analysis of a full-scale DEMON bioreactor

  2015cited by this paper
• MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities

  2015cited by this paper
• Microbial Community Composition and Ultrastructure of Granules from a Full-Scale Anammox Reactor

  2015cited by this paper
• NADPH-generating systems in bacteria and archaea

  2015cited by this paper
• Physiological characterization of anaerobic ammonium oxidizing bacterium 'Candidatus Jettenia caeni'.

  2015cited by this paper
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  2015cited by this paper
• The Transporter Classification Database (TCDB): recent advances

  2015cited by this paper
• The Pfam protein families database: towards a more sustainable future

  2015cited by this paper
• CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes

  2015cited by this paper
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  2015cited by this paper
• Bacterial formate hydrogenlyase complex

  2014cited by this paper
• PhyloSift: phylogenetic analysis of genomes and metagenomes

  2014cited by this paper
• HTSeq—a Python framework to work with high-throughput sequencing data

  2014cited by this paper
• CDD: NCBI's conserved domain database

  2014cited by this paper
• Vitamin B12 as a modulator of gut microbial ecology.

  2014cited by this paper
• Syntrophic exchange in synthetic microbial communities

  2014cited by this paper
• Genomic Analysis of Melioribacter roseus, Facultatively Anaerobic Organotrophic Bacterium Representing a Novel Deep Lineage within Bacteriodetes/Chlorobi Group

  2013cited by this paper
• The carbohydrate-active enzymes database (CAZy) in 2013

  2013cited by this paper
• Structural Basis of Biological NO Generation by Octaheme Oxidoreductases*

  2013cited by this paper
• MetaPathways: a modular pipeline for constructing pathway/genome databases from environmental sequence information

  2013cited by this paper
• Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation.

  2013cited by this paper
• How to make a living from anaerobic ammonium oxidation.

  2013cited by this paper
• Anaerobic ammonia oxidation (ANAMMOX) for side‐stream treatment of anaerobic digester filtrate process performance and microbiology

  2013cited by this paper
• Identification of the type II cytochrome c maturation pathway in anammox bacteria by comparative genomics

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• SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data

  2012cited by this paper
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  2012cited by this paper
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• Molecular mechanism of anaerobic ammonium oxidation

  2011cited by this paper
• The Pathway Tools Pathway Prediction Algorithm

  2011cited by this paper
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• FLASH: fast length adjustment of short reads to improve genome assemblies

  2011cited by this paper
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  2011cited by this paper
• Pathway Tools version 13.0: integrated software for pathway/genome informatics and systems biology

  2010cited by this paper
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  2010cited by this paper
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  2010cited by this paper
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  2010cited by this paper
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  2009cited by this paper
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