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  1. Abstract Recent research has underscored the immense diversity and key biogeochemical roles of large DNA viruses in the ocean. Although they are important constituents of marine ecosystems, it is sometimes difficult to detect these viruses due to their large size and complex genomes. This is true for “jumbo” bacteriophages, which have genome sizes >200 kbp and large capsids reaching up to 0.45 µm in diameter. In this study, we sought to assess the genomic diversity and distribution of these bacteriophages in the ocean by generating and analyzing jumbo phage genomes from metagenomes. We recover 85 marine jumbo phages that ranged in size from 201 to 498 kilobases, and we examine their genetic similarities and biogeography together with a reference database of marine jumbo phage genomes. By analyzing Tara Oceans metagenomic data, we show that although most jumbo phages can be detected in a range of different size fractions, 17 of our bins tend to be found in those greater than 0.22 µm, potentially due to their large size. Our network-based analysis of gene-sharing patterns reveals that jumbo bacteriophages belong to five genome clusters that are typified by diverse replication strategies, genomic repertoires, and potential host ranges. Our analysis of jumbo phage distributions in the ocean reveals that depth is a major factor shaping their biogeography, with some phage genome clusters occurring preferentially in either surface or mesopelagic waters, respectively. Taken together, our findings indicate that jumbo phages are widespread community members in the ocean with complex genomic repertoires and ecological impacts that warrant further targeted investigation. 
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  2. Casadesús, Josep (Ed.)
    The evolutionary forces that determine genome size in bacteria and archaea have been the subject of intense debate over the last few decades. Although the preferential loss of genes observed in prokaryotes is explained through the deletional bias, factors promoting and preventing the fixation of such gene losses often remain unclear. Importantly, statistical analyses on this topic typically do not consider the potential bias introduced by the shared ancestry of many lineages, which is critical when using species as data points because of the potential dependence on residuals. In this study, we investigated the genome size distributions across a broad diversity of bacteria and archaea to evaluate if this trait is phylogenetically conserved at broad phylogenetic scales. After model fit, Pagel’s lambda indicated a strong phylogenetic signal in genome size data, suggesting that the diversification of this trait is influenced by shared evolutionary histories. We used a phylogenetic generalized least-squares analysis (PGLS) to test whether phylogeny influences the predictability of genome size from dN/dS ratios and 16S copy number, two variables that have been previously linked to genome size. These results confirm that failure to account for evolutionary history can lead to biased interpretations of genome size predictors. Overall, our results indicate that although bacteria and archaea can rapidly gain and lose genetic material through gene transfers and deletions, respectively, phylogenetic signal for genome size distributions can still be recovered at broad phylogenetic scales that should be taken into account when inferring the drivers of genome size evolution. 
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  3. null (Ed.)
    The family Asfarviridae is a group of nucleo-cytoplasmic large DNA viruses (NCLDVs) of which African swine fever virus (ASFV) is well-characterized. Recently the discovery of several Asfarviridae members other than ASFV has suggested that this family represents a diverse and cosmopolitan group of viruses, but the genomics and distribution of this family have not been studied in detail. To this end we analyzed five complete genomes and 35 metagenome-assembled genomes (MAGs) of viruses from this family to shed light on their evolutionary relationships and environmental distribution. The Asfarvirus MAGs derive from diverse marine, freshwater, and terrestrial habitats, underscoring the broad environmental distribution of this family. We present phylogenetic analyses using conserved marker genes and whole-genome comparison of pairwise average amino acid identity (AAI) values, revealing a high level of genomic divergence across disparate Asfarviruses. Further, we found that Asfarviridae genomes encode genes with diverse predicted metabolic roles and detectable sequence homology to proteins in bacteria, archaea, and eukaryotes, highlighting the genomic chimerism that is a salient feature of NCLDV. Our read mapping from Tara oceans metagenomic data also revealed that three Asfarviridae MAGs were present in multiple marine samples, indicating that they are widespread in the ocean. In one of these MAGs we identified four marker genes with > 95% AAI to genes sequenced from a virus that infects the dinoflagellate Heterocapsa circularisquama (HcDNAV). This suggests a potential host for this MAG, which would thereby represent a reference genome of a dinoflagellate-infecting giant virus. Together, these results show that Asfarviridae are ubiquitous, comprise similar sequence divergence as other NCLDV families, and include several members that are widespread in the ocean and potentially infect ecologically important protists. 
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  4. null (Ed.)
    Giant viruses are widespread in the biosphere and play important roles in biogeochemical cycling and host genome evolution. Also known as nucleo-cytoplasmic large DNA viruses (NCLDVs), these eukaryotic viruses harbor the largest and most complex viral genomes known. Studies have shown that NCLDVs are frequently abundant in metagenomic datasets, and that sequences derived from these viruses can also be found endogenized in diverse eukaryotic genomes. The accurate detection of sequences derived from NCLDVs is therefore of great importance, but this task is challenging owing to both the high level of sequence divergence between NCLDV families and the extraordinarily high diversity of genes encoded in their genomes, including some encoding for metabolic or translation-related functions that are typically found only in cellular lineages. Here, we present ViralRecall, a bioinformatic tool for the identification of NCLDV signatures in ‘omic data. This tool leverages a library of giant virus orthologous groups (GVOGs) to identify sequences that bear signatures of NCLDVs. We demonstrate that this tool can effectively identify NCLDV sequences with high sensitivity and specificity. Moreover, we show that it can be useful both for removing contaminating sequences in metagenome-assembled viral genomes as well as the identification of eukaryotic genomic loci that derived from NCLDV. ViralRecall is written in Python 3.5 and is freely available on GitHub: https://github.com/faylward/viralrecall. 
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  5. Bordenstein, Seth (Ed.)
    ABSTRACT Viruses belonging to the Nucleocytoviricota phylum are globally distributed and include members with notably large genomes and complex functional repertoires. Recent studies have shown that these viruses are particularly diverse and abundant in marine systems, but the magnitude of actively replicating Nucleocytoviricota present in ocean habitats remains unclear. In this study, we compiled a curated database of 2,431 Nucleocytoviricota genomes and used it to examine the gene expression of these viruses in a 2.5-day metatranscriptomic time-series from surface waters of the California Current. We identified 145 viral genomes with high levels of gene expression, including 90 Imitervirales and 49 Algavirales viruses. In addition to recovering high expression of core genes involved in information processing that are commonly expressed during viral infection, we also identified transcripts of diverse viral metabolic genes from pathways such as glycolysis, the TCA cycle, and the pentose phosphate pathway, suggesting that virus-mediated reprogramming of central carbon metabolism is common in oceanic surface waters. Surprisingly, we also identified viral transcripts with homology to actin, myosin, and kinesin domains, suggesting that viruses may use these gene products to manipulate host cytoskeletal dynamics during infection. We performed phylogenetic analysis on the virus-encoded myosin and kinesin proteins, which demonstrated that most belong to deep-branching viral clades, but that others appear to have been acquired from eukaryotes more recently. Our results highlight a remarkable diversity of active Nucleocytoviricota in a coastal marine system and underscore the complex functional repertoires expressed by these viruses during infection. IMPORTANCE The discovery of giant viruses has transformed our understanding of viral complexity. Although viruses have traditionally been viewed as filterable infectious agents that lack metabolism, giant viruses can reach sizes rivalling cellular lineages and possess genomes encoding central metabolic processes. Recent studies have shown that giant viruses are widespread in aquatic systems, but the activity of these viruses and the extent to which they reprogram host physiology in situ remains unclear. Here, we show that numerous giant viruses consistently express central metabolic enzymes in a coastal marine system, including components of glycolysis, the TCA cycle, and other pathways involved in nutrient homeostasis. Moreover, we found expression of several viral-encoded actin, myosin, and kinesin genes, indicating viral manipulation of the host cytoskeleton during infection. Our study reveals a high activity of giant viruses in a coastal marine system and indicates they are a diverse and underappreciated component of microbial diversity in the ocean. 
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  6. null (Ed.)
  7. null (Ed.)
    Abstract Bacteriophages play critical roles in the biosphere, but their vast genomic diversity has obscured their evolutionary origins, and phylogenetic analyses have traditionally been hindered by their lack of universal phylogenetic marker genes. In this study we mine metagenomic data and identify a clade of Caudovirales that encodes the β and β′ subunits of multi-subunit RNA polymerase (RNAP), a high-resolution phylogenetic marker which enables detailed evolutionary analyses. Our RNAP phylogeny revealed that the Caudovirales RNAP forms a clade distinct from cellular homologs, suggesting an ancient acquisition of this enzyme. Within these multimeric RNAP-encoding Caudovirales (mReC), we find that the similarity of major capsid proteins and terminase large subunits further suggests they form a distinct clade with common evolutionary origin. Our study characterizes a clade of RNAP-encoding Caudovirales and suggests the ancient origin of this enzyme in this group, underscoring the important role of viruses in the early evolution of life on Earth. 
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  8. ABSTRACT The Thaumarchaeota is a diverse archaeal phylum comprising numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically characterized marine thaumarchaea are reported to be chemolithoautotrophic ammonia oxidizers. In this study, we report a group of putatively heterotrophic marine thaumarchaea (HMT) with small genome sizes that is globally abundant in the mesopelagic, apparently lacking the ability to oxidize ammonia. We assembled five HMT genomes from metagenomic data and show that they form a deeply branching sister lineage to the ammonia-oxidizing archaea (AOA). We identify this group in metagenomes from mesopelagic waters in all major ocean basins, with abundances reaching up to 6% of that of AOA. Surprisingly, we predict the HMT have small genomes of ∼1 Mbp, and our ancestral state reconstruction indicates this lineage has undergone substantial genome reduction compared to other related archaea. The genomic repertoire of HMT indicates a versatile metabolism for aerobic chemoorganoheterotrophy that includes a divergent form III-a RuBisCO, a 2M respiratory complex I that has been hypothesized to increase energetic efficiency, and a three-subunit heme-copper oxidase complex IV that is absent from AOA. We also identify 21 pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to supply reducing equivalents to the electron transport chain and are among the most highly expressed HMT genes, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic members of the Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations. IMPORTANCE It has been known for many years that marine Thaumarchaeota are abundant constituents of dark ocean microbial communities, where their ability to couple ammonia oxidation and carbon fixation plays a critical role in nutrient dynamics. In this study, we describe an abundant group of putatively heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from those of their ammonia-oxidizing relatives. HMT lack the ability to oxidize ammonia and fix carbon via the 3-hydroxypropionate/4-hydroxybutyrate pathway but instead encode a form III-a RuBisCO and diverse PQQ-dependent dehydrogenases that are likely used to conserve energy in the dark ocean. Our work expands the scope of known diversity of Thaumarchaeota in the ocean and provides important insight into a widespread marine lineage. 
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  9. Abstract Marine microorganisms inhabiting nutrient-depleted waters play critical roles in global biogeochemical cycles due to their abundance and broad distribution. Many of these microbes share similar genomic features including small genome size, low % G + C content, short intergenic regions, and low nitrogen content in encoded amino acid residue side chains (N-ARSC), but the evolutionary drivers of these characteristics are unclear. Here, we compared the strength of purifying selection across the Marinimicrobia, a candidate phylum which encompasses a broad range of phylogenetic groups with disparate genomic features, by estimating the ratio of nonsynonymous and synonymous substitutions (dN/dS) in conserved marker genes. Our analysis reveals that epipelagic Marinimicrobia that exhibit features consistent with genome streamlining have significantly lower dN/dS values when compared with their mesopelagic counterparts. We also found a significant positive correlation between median dN/dS values and % G + C content, N-ARSC, and intergenic region length. We did not identify a significant correlation between dN/dS ratios and estimated genome size, suggesting the strength of selection is not a primary factor shaping genome size in this group. Our findings are generally consistent with genome streamlining theory, which postulates that many genomic features of abundant epipelagic bacteria are the result of adaptation to oligotrophic nutrient conditions. Our results are also in agreement with previous findings that genome streamlining is common in epipelagic waters, suggesting that microbes inhabiting this region of the ocean have been shaped by strong selection together with prevalent nutritional constraints characteristic of this environment. 
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