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Viruses Reprogram Cells into Different Virocells

Microbial cells infected by viruses undergo metabolic reprogramming.

The Science

How a cell behaves as virocell largely depends on the infecting virus and the genomic similarity between host and virus. Pseudoalteromonas was infected with two unrelated viruses: siphovirus PSA-HS2 and podovirus PSA-HP1. The infections transformed the same bacterial host into two very different virocells, HS2-virocell and HP1-virocell. The HS2 siphovirus genome was much more similar to the host than the genome of HP1 podovirus and had better access to recycle existing host resources. In contrast, the HP1 podovirus needed to work harder at obtaining the resources needed for infection, and reprogrammed multiple host metabolisms. HS2 virocells had a comparatively higher fitness than HP1 virocells. (Figure by Cristina Howard-Varona)

How a cell behaves as virocell largely depends on the infecting virus and the genomic similarity between host and virus. Pseudoalteromonas was infected with two unrelated viruses: siphovirus PSA-HS2 and podovirus PSA-HP1. The infections transformed the same bacterial host into two very different virocells, HS2-virocell and HP1-virocell. The HS2 siphovirus genome was much more similar to the host than the genome of HP1 podovirus and had better access to recycle existing host resources. In contrast, the HP1 podovirus needed to work harder at obtaining the resources needed for infection, and reprogrammed multiple host metabolisms. HS2 virocells had a comparatively higher fitness than HP1 virocells. (Figure by Cristina Howard-Varona)

If it looks like a duck and quacks like a duck, so the adage goes, it must be a duck. But if the duck gets infected by a virus so that it no longer looks or quacks like one, is it still a duck? For a team led by researchers from The Ohio State University and the University of Michigan studying how virus infections cause significant metabolic changes in marine microbes, the answer is no. They refer to the infected microbial cells as virocells, a change in name first described in 2011 which reflects the metabolic changes they’ve undergone.

The Impact

The number of microbes in, on, and around the planet is an astronomical figure, and yet viruses outnumber them. In the ocean, viruses outnumber surface microbes 10 to 1, and 20% to 40% of the microbes are infected at any given time. Microbial viruses can thus have significant impacts on the global nutrient cycles regulated by their hosts. For example, microbes that capture and store carbon in the ocean could fix less carbon when infected. Little is known about virus-infected microbial cells that are transformed into virocells, and how the outcomes of these infections can affect the interactions within their ecosystems.

Summary

Microbes drive the energy and nutrient cycles that fuel the planet, and viruses control them through infection, but little is known about the impacts of these infections on ecosystem functions. As part of efforts to characterize global microbial diversity with an aim to improve predictive ecosystems models, University of Michigan’s Melissa Duhaime and The Ohio State University’s Matt Sullivan used an experimental approach with a marine phage-host model to study virus-host-nutrient interactions. In their study, which appeared in The ISME Journal, they focused on how virus-infected microbes are transformed into virocells that are metabolically and functionally different from uninfected cells. Duhaime and Sullivan are co-corresponding authors, while the study’s lead author is Cristina Howard-Varona, a postdoctoral researcher in Sullivan’s lab.

Their research was enabled in part by the Facilities Integrating Collaborations for User Science (FICUS) collaborative science initiative between the U.S. Department of Energy (DOE) Joint Genome Institute (JGI), a DOE Office of Science User Facility located at Lawrence Berkeley National Laboratory (Berkeley Lab), and the Environmental Molecular Science Laboratory (EMSL), a DOE Office of Science User Facility located at Pacific Northwest National Laboratory (PNNL). Researchers have the opportunity to combine the power of genomics and molecular characterization offered at multiple user facilities stewarded by the DOE’s Office of Biological and Environmental Research in one proposed research project. For this project, RNA sequencing was done by the JGI, and proteomics and metabolomics analysis and microscopy at EMSL.

The team infected the marine Pseudoalteromonas bacterium with two unrelated viruses: siphovirus PSA-HS2 and podovirus PSA-HP1. Each virus demonstrated a different approach to infecting and metabolically reprogramming the bacterial host, which was transformed into two very different virocells—HS2-virocell and HP1-virocell, respectively—and correspondingly different infection outcomes. reprogrammed the bacteria’s central carbon and energy metabolism, to obtain more nutrients from the environment.

Demonstrating that the costs of infecting microbes and their impacts on the ecosystems can vary is a step toward developing more efficient predictive ecosystems models. Next, the researchers are working towards better understanding how nutrient availability, or lack thereof, impacts viral infection and the metabolism of the resulting virocells, to better represent how infections occur in natural settings.

Letters of Intent (LOI) for FICUS collaborative research applications with EMSL and the JGI are currently being accepted until 11:00pm PDT on March 18, 2020.

Contacts:

BER Contacts
Ramana Madupu, Ph.D.
Program Manager, DOE Joint Genome Institute
Biological Systems Sciences Division
Office of Biological and Environmental Research
Office of Science
US Department of Energy
Ramana.Madupu@science.doe.gov

Paul Bayer
Program Manager, EMSL
Climate and Environmental Sciences Division
Office of Biological and Environmental Research
Office of Science
US Department of Energy
Paul.Bayer@science.doe.gov

PI Contacts

Melissa Duhaime
University of Michigan
duhaimem@umich.edu

Matt Sullivan
The Ohio State University
sullivan.948@osu.edu

Funding:

A portion of this research was performed under the Facilities Integrating Collaborations for User Science (FICUS) initiative through an award to MBD and MBS (#2582) and used resources at the DOE Joint Genome Institute and the Environmental Molecular Sciences Laboratory, which are DOE Office of Science User Facilities. Both facilities are sponsored by the Office of Biological and Environmental Research and operated under Contract Numbers DE-AC02–05CH11231 (JGI) and DE-AC05–76RL01830 (EMSL). This work was funded by a Gordon and Betty Moore Foundation Investigator Award (#3790) and an NSF Biological Oceanography award (#1536989) to MBS, University of Michigan discretionary funds to MBD, an NSF Graduate Research Fellowship to MML (#DGE1256260), as well as a National Institutes of Health (NIH)/National Institute of Allergy and Infectious Diseases (NIAID) award (#1-T32-AI-112542) to CHV. 

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By: Massie S. Ballon