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Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes - PubMed

Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes

Nathan A Ahlgren et al. ISME J. 2019 Mar.

Abstract

Much of the diversity of prokaryotic viruses has yet to be described. In particular, there are no viral isolates that infect abundant, globally significant marine archaea including the phylum Thaumarchaeota. This phylum oxidizes ammonia, fixes inorganic carbon, and thus contributes to globally significant nitrogen and carbon cycles in the oceans. Metagenomics provides an alternative to culture-dependent means for identifying and characterizing viral diversity. Some viruses carry auxiliary metabolic genes (AMGs) that are acquired via horizontal gene transfer from their host(s), allowing inference of what host a virus infects. Here we present the discovery of 15 new genomically and ecologically distinct Thaumarchaeota virus populations, identified as contigs that encode viral capsid and thaumarchaeal ammonia monooxygenase genes (amoC). These viruses exhibit depth and latitude partitioning and are distributed globally in various marine habitats including pelagic waters, estuarine habitats, and hydrothermal plume water and sediments. We found evidence of viral amoC expression and that viral amoC AMGs sometimes comprise up to half of total amoC DNA copies in cellular fraction metagenomes, highlighting the potential impact of these viruses on N cycling in the oceans. Phylogenetics suggest they are potentially tailed viruses and share a common ancestor with related marine Euryarchaeota viruses. This work significantly expands our view of viruses of globally important marine Thaumarchaeota.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1

Phylogeny of Thaumarchaeota amoC sequences from cellular Thaumarchaeota genomes and thaumarchaeal viral contigs. The tips of the tree are labeled with gene identifiers (viral contigs) or isolate or single-cell amplified genome names. Genes from contigs obtained from co-assembly of ETNP metagenomes from this study are depicted in red; genes from contigs from the Delaware and Chesapeake Bay are depicted in blue; and the locations from which all other contigs were assembled are listed after gene numbers. The tree was constructed using the HKY85 DNA substitution model with invariable sites and gamma distributed rates of evolution and heuristic search of tree space using minimum evolution as the criterion. Numbers at the nodes indicate results from bootstrap analysis (100 replicates). Bootstrap analysis supports that amoC sequences from viral contigs sequences (“Viral amoC AMG clade”) form a phylogenetically distinct clade from cellular Thaumarchaeota sequences (“Cellular Thaumarchaeota amoC”). Genes marked with stars indicate representative contigs from putative viral species delineated by average nucleotide identity (Fig. S3) that were used for measuring population abundances in various habitats (Fig. 3)

Fig. 2
Fig. 2

Contig maps depicting predicted proteins encoded on representative thaumarchaeal viral contigs. Arrows depict the location and direction of predicted proteins on contigs, and the number 1 indicates the end with first nucleotide position of the contig. Fill colors indicate different categories of genes, as indicated in the legend, according to top hits from searches against NCBI’s nr protein database or protein structure similarity analyses (Table 1). Asterisks denote which genes showed similarity to Ca. N. catalina SPOT01 putative viral gene NMSP_1228. The color of the trapezoids connecting genes indicate amino-acid identities between genes.

Fig. 3
Fig. 3

Abundance of representative Thaumarchaeota viral contigs and gene sequences in various marine samples as determined by metagenomic read mapping to a Coastal (station [stn] 2) and open-ocean (stn 6) ETNP samples from Vik et al. [33]. b Globally distributed Tara Ocean samples and c-e ETNP depth profiles from which contig ETNP_CA_420 was identified. For a–c, metagenomic reads were mapped to representative contigs from the 15 viral species. Normalized read recruitment is depicted as the number of reads mapped per kilobase of the contig per billions of reads in the sample. Contigs that did not meet the mapping criteria in any samples are not depicted in the graphs. For a and c, recruitment values are only plotted if ≥ 30 reads were mapped to the respective contig. For Tara Ocean samples in b recruitment levels are only plotted if contig coverage was ≥1 or the percentage of the contig covered was ≥75%. The following is listed for each Tara sample on the vertical axis: Tara Ocean site number, oceanic region, sampling depth, and size fraction of the sample in µm. Mesopelagic samples are in bold and blue to highlight that contig Ga0066372_10000192 was only detected in mesopelagic samples. For d, read recruitment results are shown for reads that mapped to sequences from the viral amoC AMG (“Viral amoC”) or cellular Thaumarchaeota (“Cellular amoC”) clades as defined in Fig. 1. For e, recruitment results are shown for the amoC and capsid genes on contig ETNP_CA_420

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References

    1. Könneke M, Bernhard AE, De La Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 2005;437:543–6. doi: 10.1038/nature03911. - DOI - PubMed
    1. Könneke M, Schubert DM, Brown PC, Hugler M, Standfest S, Schwander T, et al. Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation. Proc Natl Acad Sci USA. 2014;111:8239–44. doi: 10.1073/pnas.1402028111. - DOI - PMC - PubMed
    1. Walker CB, De La Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA. 2010;107:8818–23. doi: 10.1073/pnas.0913533107. - DOI - PMC - PubMed
    1. Santoro AE, Casciotti KL, Francis CA. Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ Microbiol. 2010;12:1989–2006. doi: 10.1111/j.1462-2920.2010.02205.x. - DOI - PubMed
    1. Beman JM, Popp BN, Francis CA. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J. 2008;2:429–41. doi: 10.1038/ismej.2007.118. - DOI - PubMed

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