Chris Francis

Associate Professor of Earth System Science

Address:
Earth System Science
473 Via Ortega, Y2E2 Building
Stanford University
Stanford, CA 94305-4216

Phone: (650) 724-0301
Fax: (650) 725-2199

Research

Education and Experience

Publications

Research Group

LINKS

Francis CV

ESS Department

School of Earth, Energy & Environmental Sciences

Hopkins Microbiology Course

Research

My research interests center on the molecular, biochemical, and ecological aspects of the microbial geochemical cycling of nitrogen and metals in the environment.   I am particularly interested in determining the key organisms, functional genes, and molecular mechanisms underlying these biogeochemical processes through both laboratory and field studies.

MICROBIAL NITROGEN CYCLING

Nitrification. The oxidation of NH₃ to NO₂^- and ultimately NO₃^- by chemoautotrophic nitrifying bacteria [ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB), respectively] is a critical branch of the nitrogen cycle in soil, sedimentary, marine, freshwater and estuarine environments, where this process provides a key link between the mineralization of organic nitrogen and the subsequent loss of fixed nitrogen via denitrification and anammox. Much of our research is focused on exploring the diversity and structure of ammonia-oxidizing microbial communities, based on amoA gene sequences encoding the alpha-subunit of the key nitrification enzyme, ammonia monooxygenase (AMO). Our work has revealed the widespread occurrence of the previously unrecognized group of ammonia-oxidizing archaea (AOA) in marine water columns and sediments. We are currently using molecular and biogeochemical approaches to explore the relative diversity, abundance, and activity of AOA and AOB in a number of marine and estuarine systems, including the central California Current System, Monterey Bay, the Gulf of California/Eastern Tropical North Pacific, the Elkhorn Slough estuary, and San Francisco Bay, among others. In addition, we are using cultivation, metagenomic and (meta)transcriptomic approaches to gain a deeper understanding of the genetic and physiological basis for thaumarchaeal ammonia oxidation in natural systems.

Transmission electron micrograph of Nitrosoarchaeum limnia SFB1, a novel ammonia-oxidizing archaeon isolated from low-salinity sediments in the San Francisco Bay estuary (see Blainey/Mosier et al., 2011; Mosier et al., 2012)

Denitrification. The dissimilatory reduction of nitrate and nitrite to gaseous products (NO, N₂O, N₂) under suboxic conditions, denitrification, is a major loss term for fixed nitrogen from ecosystems. This process removes up to 50% of external N inputs from estuarine and coastal sediments, and also leads to the production of potent greenhouse gases, NO and N₂O. Despite the global importance of denitrifiers, the "key players" in most environments are simply not known. Functional genes encoding key metalloenzymes in the denitrification pathway have proven to be useful molecular markers for the environmental detection of denitrifiers. Our work has focused on characterizing the distribution, diversity, abundance, and acitivity of denitrifiers across physical/chemical gradients in many of the environments where we are also studying ammonia-oxidizers (e.g., Elkhorn Slough, San Francisco Bay, GOC/ETNP, etc.). By simultaneously examining these two key branches of the microbial N cycle, we hope to gain new insights into the relationships betwen functional diversity, environmental gradients, and biogeochemical function.

Diagram of the marine microbial nitrogen cycle, with key processes and functional genes studied in the Francis Laboratory highlighted in bold or yellow, respectively (modified from a figure that appeared in Francis et al., 2007).

MICROBIAL METAL CYCLING

Manganese(II) Oxidation. The oxidation of soluble manganese(II) to insoluble Mn(III,IV) oxides is an environmentally important process because the solid phase products oxidize a variety of organic and inorganic compounds [e.g., humics, Cr(III), Fe(II), HS-], scavenge many heavy metals (e.g., Cu, Co, Cd, Zn, Ni, Pb), and serve as electron acceptors for anaerobic respiration. Although most of the Mn(II) oxidation which occurs in the environment is microbially-mediated, the diversity of organisms responsible for this activity and the underlying mechanisms of catalysis remain poorly understood.  My previous work revealed that Mn(II)-oxidizing bacteria are phylogenetically diverse and that multicopper oxidases (MCOs) appear to play a widespread role in Mn(II) oxidation. However, we still know very little regarding which organisms are responsible for Mn(II) oxidation in nature. Our current research is focused on using molecular and cultivation-based approaches to characterize the diversity and physiology of Mn(II)-oxidizing bacteria in freshwater, estuarine, and marine environments.

Biogenic Mn oxide-encrusted sediments in a small California estuary

Dissimilatory Metal Reduction.  Along with metal oxdation, we are also interested in microbes capable of coupling anaerobic growth to the dissimilatory reduction of various metals, including Mn(VI), Fe(III), U(VI), and As(V) in soils and sediments. In addition, we are currently working on a collaborative project examining how microbial N cycling influences the fate and transport of uranium in subsurface systems (see SLAC SFA).

Education and Experience

Education

Ph.D., 2000, Marine Biology, Scripps Institution of Oceanography, University of California, San Diego

Summer Course, 1998, Microbial Diversity, Marine Biological Laboratory, Woods Hole, MA

Employment

2011-present Senior Fellow, Woods Institute for the Environment, Stanford University

2010-present Associate Professor of Earth System Science, Stanford University

2008-present Assistant Professor of Environmental Earth System Science, Stanford University

2003-2008 Assistant Professor of Geological & Environmental Sciences, Stanford University

2002-2003 NSF Postdoctoral Research Fellow in Microbial Biology, Department of Geosciences, Princeton University

2001 Harry Hess Postdoctoral Fellow in Geosciences, Department of Geosciences, Princeton University

Publications (since 1998)

Francis, C. A., A. K. Francis, D. Golet, and B. B Ward. 1998. Quantification of catechol 2,3-dioxygenase gene homology and benzoate utilization in intertidal sediments. Aquatic Microbial Ecology 15: 225-231.

Tebo, B. M., L. van Waasbergen, C. A. Francis, L. M. He, D. B. Edwards, and K. Casciotti. 1998. Manganese oxidation by spores of the marine Bacillus sp. strain SG-1: Application for the bioremediation of metal pollution. In Y. Le Gal and H.O. Halvorson (Eds.) New Developments in Marine Biotechnology. Plenum Press, New York. p.177-180.

Francis, C. A., and B. M. Tebo. 1999. Marine Bacillus spores as catalysts for oxidative precipitation and sorption of metals. Journal of Molecular Microbiology and Biotechnology 1: 71-78.

Francis, C. A., A. Y. Obraztsova, and B. M. Tebo. 2000. Dissimilatory metal reduction by the facultative anaerobe Pantoea agglomerans SP1. Applied and Environmental Microbiology 66: 543-548.

Francis, C. A., and B. M. Tebo. 2000. Marine Bacillus spores as catalysts for the oxidative precipitation and sorption of metals. In D.H. Bartlett (Ed.) Molecular Marine Microbiology. Horizon Scientific Press, Norfolk, England.

Francis, C. A., and B. M. Tebo. 2001. cumA multicopper oxidase genes from diverse Mn(II) oxidizing and non-Mn(II)-oxidizing Pseudomonas strains. Applied and Environmental Microbiology 67: 4272-4278.

Francis, C. A., E.-M. Co, and B. M. Tebo. 2001. Enzymatic manganese(II) oxidation by a marine a-proteobacterium. Applied and Environmental Microbiology 67: 4024-4029.

Francis, C. A. , and B. M. Tebo. 2002. Enzymatic manganese(II) oxidation by metabolically dormant spores of diverse Bacillus species. Applied and Environmental Microbiology 68: 874-880.

Obraztsova, A. Y., C. A. Francis, and B. M. Tebo. 2002. Sulfur disproportionation by the facultative anaerobe Pantoea agglomerans as a mechanism for chromium(VI) reduction. Geomicrobiology Journal 19: 121-132.

Francis, C. A., K. L. Casciotti, and B. M. Tebo. 2002. Localization of Mn(II)-oxidizing activity and the putative multicopper oxidase, MnxG, to the exosporium of the marine Bacillus sp. strain SG-1. Archives of Microbiology 178:450-456.

Taroncher-Oldenburg, G., E. M. Griner, C. A. Francis, and B. B. Ward. 2003. Oligonucleotide microarray for the study of functional gene diversity in the nitrogen cycle in the environment. Applied and Environmental Microbiology 69:1159-1171.

Francis, C. A., G. D. O'Mullan, and B. B. Ward.  2003. Diversity of ammonia monooxygnenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiology 1:129-140.

Jayakumar, D. A., C. A. Francis, S. W. A. Naqvi, and B. B. Ward. 2004. Diversity of nitrite reductase genes (nirS) in the denitrifying water column of the coastal Arabian Sea. Aquatic Microbial Ecology 34:69-78.

Francis, C. A., K. J. Roberts, J. M. Beman, A. E. Santoro, and B. B. Oakley. 2005. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences 102:14683-14688.

Santoro, A. E., A. B. Boehm, and C. A. Francis. 2006. Denitrifier community composition along a nitrate and salinity gradient in a coastal aquifer. Applied and Environmental Microbiology 72:2102-2109.

Glatz., R. E., P. W. Lepp, B. B. Ward, and C. A. Francis. 2006. Planktonic microbial community composition across steep physical/chemical gradients in permanently ice-covered Lake Bonney, Antarctica. Geobiology 4:53-67.

Hansel, C. M., and C. A. Francis. 2006. Coupled Mn(II) oxidation pathways of a planktonic Roseobacter-like bacterium. Applied and Environmental Microbiology 72:3543-3549.

Research Group

(left to right) : Shellie Bench (former postdoc), Jessica Lee (former PhD student; now postdoc, University of Idaho), Emily Cardarelli (PhD student), Bradley Tolar (postdoc), Julian Damashek (PhD student), Chris Francis, and Linta Reji (PhD student). February 2015.

Front Row (left to right) : Chris Francis, Alyson Santoro (currently Assistant Professor, UMCES-Horn Point Laboratory), Samantha Ying (currently Assistant Professor, UC Riverside), Mike Beman (currently Assistant Professor, UC Merced); Back Row: Colleen Hansel (currently Associate Scientist, Woods Hole Oceanographic Institution), Scott Wankel (currently Assistant Scientist, Woods Hole Oceanographic Institution), Annika Mosier (currently Assistant Professor, University of Colorado Denver), George Wells (currently Assistant Professor, Northwestern University). Students and postdocs not shown: Steve Biller (currently postdoctoral fellow, MIT-Chisholm Lab), Emily Cardarelli, Julian Damashek, Jessica Lee, Marie Lund, and Jason Smith (currently MBARI Postdoctoral Fellow).