Lab: Life Sciences South 203/207
Phone: (520) 626-6297
Research in the Tucson Marine Phage Lab
Broadly we are interested in the the ecology and evolution of natural systems. Our focus is on how ocean viruses, as tiny but abundant biological entities, impact global biogeochemical cycles through interactions with their microbial hosts' core metabolic functions.
To this end, we leverage an experimental model-systems approach with the application of modern techniques as phenomenologically-revealing windows into 'wild' viral populations. Three TMPL research directions include:
- Model system development (Cyanophages and "Heterophages")
- Tool development (The Biosphere 2 Ocean)
- Field work:
- Viral biogeography: Project OViD: Ocean Virus Diversity in the context of the Tara Oceans and Malaspina global oceanographic research expeditions
- Coastal to open ocean transects (the subarctic North Pacific Ocean, LineP; MBARI's Line67)
- Extreme environments (3km deep hypersaline pools)
Cyanophages: A model for studying global-scale photosynthetic host-phage interactions in the oceans
The marine cyanobacteria Prochlorococcus and Synechococcus are globally important primary producers. In spite of their small size, these cyanobacterial cells are numerically dominant over vast areas of the "desert oceans" and are significant contributors to global carbon cycling. These were some of the earliest "ecological microbes" sequenced by the DOE JGI, which led to an understanding of the genomic underpinnings that are responsible for their ecological niches in the environment (Jed Fuhrman's News and Views, research articles Rocap et al. 2003, Palenik et al 2003).
Cyanobacterial viruses (cyanophages) are abundant, contribute to host mortality, and impact marine cyanobacterial diversity through mortality and moving genes through the host population. Cyanophage genomes appear to be standard "coliphage" decorated with a suite of niche- and host-defining genes. These latter genes include photosynthesis genes, as well as genes likely involved in carbon metabolism, phosphate stress and novel nucleotide metabolism genes. Detailed studies of the core reaction center genes suggest that they are widespread among cyanophage isolates with a seemingly predictable distribution, they are expressed during infection, and parts of the viral copies of the genes have even been transferred back into their hosts - thus cyanophages are acting as evolutionary drivers of the core reaction centers of the numerically dominant photosystems on the planet.
The oceanic cyanophage collection I developed at MIT contains over 1000 plaque-purified strains systematically isolated using a diversity of Prochlorococcus and Synechococcus host strains and source waters. Model cyanophage strains that have been used in experimental work have been characterized to varying degrees, while the remainder phage strains remain uncharacterized but an ideal reagent for large-scale screens.
At the University of Arizona, I am continuing cyanophage work. If you are interested in cyanophages, please inquire about available projects.
For details on cyanophages from my thesis and post-doctoral work, please see these selected publications.
"Heterophages": Towards new globally-important phage-host model systems
The role of heterotrophic bacteria and their phages has been underexplored in the wild. We are interested in using genomically-characterized representative host strains to develop novel phage-host model systems that can be used for hypothesis testing in non-photosynthetic (e.g., heterotrophic) microbes.
Using DOE- and Gordon and Betty Moore Foundation funding, three model systems are currently under development: Pseudoalteromonas (by Melissa Duhaime) and Cellulophaga (by Karin Holmfeldt) marine phages, and a diversity of freshwater cyanophages (by Li Deng). Do ocean heterophage and freshwater cyanophage genomes evolve in parallel ways (gene content, ortholog sequence conservation, etc) to their marine cyanophage counterparts? Do heterophages similarly impact global biogeochemical cycles, or might their biogeochemical domain be more focused on other critical elements like nitrogen or sulfur?
The Biosphere 2 Ocean: Developing new tools for interrogating 'wild' viral populations
The young field of ocean viral ecology suffers from a lack of available tools that are needed to elucidate the inner workings of the complex, interconnected viral populations in the 'wild'. With the emergence of single-particle toolkits (e.g., microfluidics, flow cytometry, 'omics'), a new window into the variability of individuals in populations offers the promise of unprecedented insight. The Biosphere 2 Ocean offers TMPL an accessible (<1 hours drive from Tucson) and diverse aquatic field site for studying 'wild' microbial and viral populations. This proximity to such a site provides both the opportunity for temporal and spatial characterization of these communities, as well as naturally complex source waters for evaluation of new tools for interrogating 'wild' populations.
Our B2-, NSF- and Gordon and Betty Moore Foundation-funded research into building new tools for viral ecology currently features methods for viral concentration, viral metagenomic library construction , and molecular tagging.
Video overview of Biosphere 2. The Ocean is featured about 2/3 of the way through.
The Arizona Daily Star featured the TMPL-guided undergraduate project to survey the overall ecology and fish populations of the B2 ocean.
Undergraduate "Fish Gang" project blog
Field work for viral biogeography: Project OViD: Ocean Virus Diversity in the context of the Tara Oceans and Malaspina global oceanographic research expeditions
Sampling details available here
In Project OViD (Ocean Virus Diversity), we explore the diversity, phylogeography and genomic variability of the most abundant ocean viral group known to date: the T4-like viruses.
TMPL is amassing an unprecedented archive of systematically-collected, metadata-rich ocean viral concentrates from two European-funded global oceanographic research expeditions, Tara Oceans and Malaspina. In total, we anticipate > 2,000 samples from multiple depths at 550 sites around the world’s oceans. Both expeditions explore the biology, chemistry, and physics of the oceans through large, international consortiums that include unprecedentedly diverse expertise. Further, both consortiums are built upon open exchange of ideas, well-documented voucher collections, and robust databasing to support sample archives. This is a foundation for diversity studies on a scale not previously possible.
Tara Oceans |
Malaspina |
|
|---|---|---|
| Dates | Sept 2009 to Nov 2012 |
Oct 2010 to June 2011 |
| Stations | 375 |
180 |
| Sampled stations already at UA | 75 |
0 |
| Depths | 1 to 5 per station; to 1000m |
9 per station; to 5000m |
| Ocean zones sampled | Mostly photic zone |
Photic zone and deep sea |
| Scientists directly involved | ~200 |
~300 |
| Countries | France led, 50 labs in 15 countries |
Spain led, 30 labs in 14 countries |
| Scientists on board | 5 at a time, rotating ~monthly |
29 per leg, rotating ~monthly |
| European financing to date | $35M |
$10M |
Cruise tracks of the Tara Oceans and Malaspina expeditions. Tara Oceans cruise track is highlighted in blue (2009-2010),
green (2010-2011), and white (2011-2012) lines, while that of the 10-month Malaspina expedition is red.
Tara Oceans Expedition web site
Overview of Tara Oceans mission in PLoS Biology
Tara Oceans station data (login required)
Malaspina Expedition web site (Spanish language)
Malaspina Expedition interactive map
Nature newsblog: Malaspina expedition: Shipping out - February 11, 2011
Nature News: Spain's ship comes in (July 5, 2011)
Field work along coastal- to open-ocean transects: Line P and Line67

Line P (collaborative with Prof. Steven Hallam, UBC, Canada)
The subarctic Eastern North Pacific (ENP) Ocean hosts a massive, deep-water oxygen minimum zone (OMZ), and large annual open-ocean dimethylsulfide (DMS) pulses. Marine OMZs are sources for climatologically active trace gases including methane, nitrous oxide, and dimethylsulfide, and major sinks for nitrogen. Microbially-mediated biological activity within these systems thus directly impacts both ocean productivity and global climate balance. In addition, ENP surface waters see large annual blooms of phytoplankton and bloom-associated bacteria that generate significant fluxes of DMS, which when 'leaked' to the atmosphere influences global climate through cloud formation. The LineP transect of the ENP OMZ has been oceanographically monitored for >50 years, and in recent years has adopted a microbiological research focus.
Our DOE- and NSF-funded research seeks to explore the roles that viruses play in these systems, in the context of the Hallam Lab's microbial prokaryote work. What types of viruses are there, and how are they distributed throughout 4,000m of the water column? What microbial metabolisms might they be manipulating (e.g., photosynthesis)? How do their communities change over space and time?
Line67 (collaborative with Dr. Alex Worden, MBARI, USA)
The Line67 transect was initiated ~1950 as part of the CalCOFI program and is a designated time series site with over 20 years of contextual data maintained between MBARI and Scripps Institution of Oceanography. This coastal- to open-ocean transect traverses a Monterey Bay coastal area influenced by agricultural runoff, natural mesotrophic waters, and oligotrophic waters -- all through one of the most well-known and well-studied upwelling regions in the world, the Monterey Bay.
Our DOE-funded research focuses on studying how viral communities change along this oceanographically rich transect, as well as how viruses impact their microbial prokaryote and picoeukaryote hosts.
Field work: Extreme environments
Deep hypersaline pools (collaborative with Prof. Michail Yakimov, IAMC, Italy)
Buried 3,000m deep beneath the eastern Mediterannean Sea are extreme hypersaline pools that are saturated with either 5M NaCl or 6M MgCl2). Remarkably, microbial life exists here and functions, and scientists at the IAMC in Italy have figured out how sample not only within these hypersaline pools, but also with incredible accuracy (10s of centimeters) across the *interface* between the deep seawater and hypersaline pool waters. We hope to develop methods to create viral concentrates and metagenomic libraries from these challenging samples.

