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Phytoplankton viruses facilitate the production of dissolved organic matter (DOM) through host lysis, shaping DOM composition, and subsequent regenerative processing. We explored how DOM generated from a bloom-forming, centric diatom, infected with taxonomically distinct viruses—a single-stranded (ss) DNA and a ssRNA virus—impacted microbial processing of organic matter. DOM derived from uninfected and ssDNA virus–infected cultures supported growth in bacterial isolates and a mixed assemblage. In contrast, DOM from ssRNA virus infection did not stimulate growth, but rather induced ectoproteolytic activity, suggesting this DOM was less bioavailable. Exoprotease activity was also substantially higher in ssRNA virus–infected cellular exudates compared to ssDNA virus–infected and uninfected cultures. This suggests that DOM produced through virus-mediated host lysis does not a priori support secondary production and implicate ssRNA virus infection as a source of proteolytic activity in the water column, highlighting a multifaceted role for viruses in altering microbial utilization and remineralization length scales of organic matter in the ocean.
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Environment-specific virocell metabolic reprogramming
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.
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- Award ID(s):
- 2019589
- PAR ID:
- 10559573
- Publisher / Repository:
- Nature Portfolio
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 18
- Issue:
- 1
- ISSN:
- 1751-7362
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/ismejo/wrae055
