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. 2017 Apr 6;12(4):e0174930.
doi: 10.1371/journal.pone.0174930. eCollection 2017.

Assessing biosynthetic potential of agricultural groundwater through metagenomic sequencing: A diverse anammox community dominates nitrate-rich groundwater

William B Ludington  1 , Thaddeus D Seher  1 , Olin Applegate  2 , Xunde Li  3   4 , Joseph I Kliegman  5 , Charles Langelier  5 , Edward R Atwill  3   4 , Thomas Harter  2 , Joseph L DeRisi  5   6
Affiliations

Assessing biosynthetic potential of agricultural groundwater through metagenomic sequencing: A diverse anammox community dominates nitrate-rich groundwater

William B Ludington et al. PLoS One. .

Abstract

Background: Climate change produces extremes in both temperature and precipitation causing increased drought severity and increased reliance on groundwater resources. Agricultural practices, which rely on groundwater, are sensitive to but also sources of contaminants, including nitrate. How agricultural contamination drives groundwater geochemistry through microbial metabolism is poorly understood.

Methods: On an active cow dairy in the Central Valley of California, we sampled groundwater from three wells at depths of 4.3 m (two wells) and 100 m (one well) below ground surface (bgs) as well as an effluent surface water lagoon that fertilizes surrounding corn fields. We analyzed the samples for concentrations of solutes, heavy metals, and USDA pathogenic bacteria of the Escherichia coli and Enterococcus groups as part of a long term groundwater monitoring study. Whole metagenome shotgun sequencing and assembly revealed taxonomic composition and metabolic potential of the community.

Results: Elevated nitrate and dissolved organic carbon occurred at 4.3m but not at 100m bgs. Metagenomics confirmed chemical observations and revealed several Planctomycete genomes, including a new Brocadiaceae lineage and a likely Planctomycetes OM190, as well novel diversity and high abundance of nano-prokaryotes from the Candidate Phyla Radiation (CPR), the Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaea (DPANN) and the Thaumarchaeota, Aigarchaeota, Crenarchaeota, Korarchaeota (TACK) superphyla. Pathway analysis suggests community interactions based on complimentary primary metabolic pathways and abundant secondary metabolite operons encoding antimicrobials and quorum sensing systems.

Conclusions: The metagenomes show strong resemblance to activated sludge communities from a nitrogen removal reactor at a wastewater treatment plant, suggesting that natural bioremediation occurs through microbial metabolism. Elevated nitrate and rich secondary metabolite biosynthetic capacity suggest incomplete remediation and the potential for novel pharmacologically active compounds.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Dairy schematic.
Cartoon of the sampling sites. (A) Roughly to scale layout of the sampling sites along with land use practices. (B) Illustration of vertical distribution of sampling sites. Wells, depths, and approximate characteristics of the aquifer are depicted.
Fig 2
Fig 2. Homology of assembled Brocadiaceae genomes to the Jettenia caeni reference genome.
BRIG [37] was used to compare the Brocadiaceae genomic bins to the reference Jettenia caeni by BLASTN [38]. Radial colored bars in the concentric rings indicate nucleotide homology (30–100%). See graphical legend for ring identities. MW5 bins are shown in green, MW6 in red, and DOM in blue. Contig order is that of the reference genome.
Fig 3
Fig 3. VizBin-based clustering of contigs based on the pentanucleotide (5-mer) frequency distribution shows distinct anammox genomes.
Each dot indicates a specific contig 1000 to 5000 bp in length. Color code in the key indicates identity of the dots by shape and color.
Fig 4
Fig 4. 16S phylogeny of the Planctomycetes on shows diversity within two distinct groups, the Brocadiaceae and the OM190 clade.
Bold samples indicate they are from this study. Scale bar indicates 10% sequence divergence.
See this image and copyright information in PMC

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