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Abstract Viruses impact microbial systems through killing hosts, horizontal gene transfer, and altering cellular metabolism, consequently impacting nutrient cycles. A virus-infected cell, a “virocell,” is distinct from its uninfected sister cell as the virus commandeers cellular machinery to produce viruses rather than replicate cells. Problematically, virocell responses to the nutrient-limited conditions that abound in nature are poorly understood. Here we used a systems biology approach to investigate virocell metabolic reprogramming under nutrient limitation. Using transcriptomics, proteomics, lipidomics, and endo- and exo-metabolomics, we assessed how low phosphate (low-P) conditions impacted virocells of a marine Pseudoalteromonas host when independently infected by two unrelated phages (HP1 and HS2). With the combined stresses of infection and nutrient limitation, a set of nested responses were observed. First, low-P imposed common cellular responses on all cells (virocells and uninfected cells), including activating the canonical P-stress response, and decreasing transcription, translation, and extracellular organic matter consumption. Second, low-P imposed infection-specific responses (for both virocells), including enhancing nitrogen assimilation and fatty acid degradation, and decreasing extracellular lipid relative abundance. Third, low-P suggested virocell-specific strategies. Specifically, HS2-virocells regulated gene expression by increasing transcription and ribosomal protein production, whereas HP1-virocells accumulated host proteins, decreased extracellular peptide relative abundance, and invested in broader energy and resource acquisition. These results suggest that although environmental conditions shape metabolism in common ways regardless of infection, virocell-specific strategies exist to support viral replication during nutrient limitation, and a framework now exists for identifying metabolic strategies of nutrient-limited virocells in nature. 

Abstract With rising global temperatures, permafrost carbon stores are vulnerable to microbial degradation. The enzyme latch theory states that polyphenols should accumulate in saturated peatlands due to diminished phenol oxidase activity, inhibiting resident microbes and promoting carbon stabilization. Pairing microbiome and geochemical measurements along a permafrost thaw-induced saturation gradient in Stordalen Mire, a model Arctic peatland, we confirmed a negative relationship between phenol oxidase expression and saturation but failed to support other trends predicted by the enzyme latch. To inventory alternative polyphenol removal strategies, we built CAMPER, a gene annotation tool leveraging polyphenol enzyme knowledge gleaned across microbial ecosystems. Applying CAMPER to genome-resolved metatranscriptomes, we identified genes for diverse polyphenol-active enzymes expressed by various microbial lineages under a range of redox conditions. This shifts the paradigm that polyphenols stabilize carbon in saturated soils and highlights the need to consider both oxic and anoxic polyphenol metabolisms to understand carbon cycling in changing ecosystems. 

Summary Bacteriophages encode host‐acquired functional genes known as auxiliary metabolic genes (AMGs). Photosynthesis AMGs are commonly found in marine cyanobacteria‐infectingMyoviridaeandPodoviridaecyanophages, but their ecology remains understudied in freshwater environments. To advance knowledge of this issue, we analysed viral metagenomes collected in the summertime for four years from five lakes and two estuarine locations interconnected by the Chattahoochee River, Southeast USA. Sequences representing ten different AMGs were recovered and found to be prevalent in all sites. Most freshwater AMGs were 10‐fold less abundant than estuarine and marine AMGs and were encoded by novelMyoviridaeandPodoviridaecyanophage genera. Notably, several of the corresponding viral genomes showed endemism to a specific province along the river. This translated intopsbAgene phylogenetic clustering patterns that matched a marine vs. freshwater origin indicating thatpsbAmay serve as a robust classification and source‐tracking biomarker. Genomes classified in a novel viral lineage represented by isolate S‐EIVl containedpsbA, which is unprecedented for this lineage. Collectively, our findings indicated that the acquisition of photosynthesis AMGs is a widespread strategy used by cyanophages in aquatic ecosystems, and further indicated the existence of viral provinces in which certain viral species and/or genotypes are locally abundant. 

Summary Oxygen minimum zones (OMZs) are critical to marine nitrogen cycling and global climate change. While OMZ microbial communities are relatively well‐studied, little is known about their viruses. Here, we assess the viral community ecology of 22 deeply sequenced viral metagenomes along a gradient of oxygenated to anoxic waters (<0.02 μmol/l O₂) in the Eastern Tropical South Pacific (ETSP) OMZ. We identified 46 127 viral populations (≥5 kb), which augments the known viruses from ETSP by 10‐fold. Viral communities clustered into six groups that correspond to oceanographic features. Oxygen concentration was the predominant environmental feature driving viral community structure. Alpha and beta diversity of viral communities in the anoxic zone were lower than in surface waters, which parallels the low microbial diversity seen in other studies. ETSP viruses were largely endemic, with the majority of shared viruses (87%) also present in other OMZ samples. We detected 543 putative viral‐encoded auxiliary metabolic genes (AMGs), of which some have a distribution that reflects physico‐chemical characteristics across depth. Together these findings provide an ecological baseline for viral community structure, drivers and population variability in OMZs that will help future studies assess the role of viruses in these climate‐critical environments.