Associate Professor of Environmental Earth System Science
Phone: (650) 724-0301
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 chemolithoautotrophic 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 a-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 and genomic approaches to gain a deeper understanding of the genetic and physiological basis for crenarchaeal ammonia oxidation in natural systems.
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).
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, but also leads to the accumulation of potent greenhouse gases, NO and N2O, which also contribute to the destruction of the stratospheric ozone layer. 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 recent 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 in the same ecosystem(s), we hope to gain new insights into the relationships betwen functional diversity, environmental gradients, and biogeochemical function.
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 universal 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. Of particular interest, one of our coastal planktonic Mn(II)-oxidzing isolates (strain AzwK-3b) has been sequenced through the Gordon and Betty Moore Foundation's Microbial Genome Sequencing Project (http://www.moore.org/microgenome/).
Biogenic Mn oxide-encrusted sediments in a small California estuary
Dissimilatory Metal Reduction. In addition to metal oxdation, we are also interested in bacteria capable of coupling anaerobic growth to the reduction of various metals, including Mn(VI), Fe(III), U(VI), and As(V) in soils and sediments.
Ph.D., 2000, Marine Biology, Scripps Institution of Oceanography, University of California, San Diego
Summer Course, 1998, Microbial Diversity, Marine Biological Laboratory, Woods Hole, MAB.A., 1994, Biology (Highest Honors), University of California, Santa Cruz
2011-present Senior Fellow, Woods Institute for the Environment, Stanford University
2010-present Associate Professor of Environmental 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
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.
Wankel, S. D., C. Kendall, C. A. Francis, and A. Paytan. 2006. Nitrogen sources and cycling in the San Francisco Bay Estuary: A nitrate dual isotopic composition approach. Limnology and Oceanography 51:1654-1664.
Park, H-D., G. F. Wells, H. Bae, C. S. Criddle, and C. A. Francis. 2006. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Applied and Environmental Microbiology 72: 5643-5647.
Beman, J. M., and C. A. Francis. 2006. Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahia del Tobari, Mexico. Applied and Environmental Microbiology 72:7767-7777.
Oakley, B. B., C. A. Francis., K. J. Roberts, C. A. Fuchsman, S. Srinivasan, and J. T. Staley. 2007. Analysis of nitrite reductase (nirK and nirS) genes and cultivation reveal depauperate community of denitrifying bacteria in the Black Sea suboxic zone. Environmental Microbiology 9: 119-130.
Francis, C. A., J. M. Beman, and M. M. M. Kuypers. 2007. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME Journal 1: 19-27.
Beman, J. M., K. J. Roberts, L. Wegley, F. Rohwer, and C.A. Francis. 2007. Distribution and diversity of archaeal ammonia monooxygenase (amoA) genes associated with corals. Applied and Environmental Microbiology 73:5642-5647.
Spear, J. R., H. A. Barton, C. E. Robertson, C. A. Francis, and N. R. Pace. 2007. Microbial community biofbrics in a geothermal mine adit. Applied and Environmental Microbiology 73:6172-6180.
Hansel, C. M., S. Fendorf, P. M. Jardine, and C. A. Francis. 2008. Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Applied and Environmental Microbiology 74:1620-1633.
Santoro, A. E., C. A. Francis, N. R. de Sieyes, and A. B. Boehm. 2008. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environmental Microbiology 10:1068-1079.
Beman, J. M., B. N. Popp, and C. A. Francis. 2008. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. The ISME Journal 2:429-441.
Mosier, A. C., and C. A. Francis. 2008. Relative abundance of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environmental Microbiology 10:3002-3016.
Bulow, S. E., C. A. Francis, G. A. Jackson, and B. B. Ward. 2008. Sediment denitrifier community composition and nirS gene expression investigated with functional gene microarrays. Environmental Microbiology 10:3057-3069.
Wells, G. F., H-D. Park, C-H. Yeung, B. Eggleston, C. A. Francis, and C. S. Criddle. 2009. Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environmental Microbiology 11:2310-2328.
Santoro, A. E., K. L. Casciotti, and C. A. Francis. 2010. Activity, abundance, and diversity of nitrifying archaea and bacteria in the central California Current. Environmental Microbiology 12: 1989-2006.
Mosier, A. C., and C. A. Francis. 2010. Denitrifier abundance and activity across the San Francisco Bay estuary. Environmental Microbiology Reports 2: 667-676..
Reed, D. W., J. M. Smith, C. A. Francis, and Y. Fujita. 2010. Response of ammonia-oxidizing bacterial and archaeal populations to organic nitrogen amendments in low-nutrient groundwater. Applied and Environmental Microbiology 76:2517-2523.
Ofiteru, I. D., M. Lunn, T. P. Curtis, G. F. Wells, C. S. Criddle, C. A. Francis, and W. T. Sloan. 2010. Combined niche and neutral effects in a microbial wastewater treatment community. Proceedings of the National Academy of Sciences 107: 15345-15350.
Wankel, S. D., A. C., Mosier, C. M. Hansel, A. Paytan, and C. A. Francis. 2011. Spatial variability in nitrification rates and ammonia-oxidizing microbial communities in the agriculturally impacted Elkhorn Slough estuary. Applied and Environmental Microbiology 77: 269-280.
Mosier, A. C., and C. A. Francis. 2011. Determining the distribution of marine and coastal ammonia-oxidizing archaea and bacteria using a quantitative approach. Methods in Enzymology 486: 205-221.
*Blainey, P. C. , A. C. Mosier*, A. Potanina, C. A. Francis, and S. R. Quake. 2011. Genome of a low-salinity ammonia-oxidizing archaeon determined by sinlge-cell and metagenomic analysis PLoS ONE 6: e16626. (* = authors contributed equally)
Pitcher, A., E. C. Hopmans, A. C. Mosier, S J. Park, S. K. Rhee, C. A. Francis, S. Schouten S, and J.S. Sinninghe Damsté. 2011. Core and intact polar glycerol dibiphytanyl glycerol tetraether lipids of ammonia-oxidizing Archaea enriched from marine and estuarine sediments. Applied and Environmental Microbiology 77: 3468-3477.
Wells, G. F., H-D. Park, B. Eggleston, C. A. Francis, and C. S. Criddle. 2011. Fine-scale bacterial community dynamics and the taxa–time relationship within a full-scale activated sludge bioreactor. Water Research 45: 5476-5488.
Robidart J. C., C. M. Preston, R. W. Paerl, K. A. Turk, A. C. Mosier, C. A. Francis, C. A. Scholin, and J. P. Zehr. 2012. Seasonal Synechococcus and Thaumarchaeal population dynamics examined with high resolution with remote in situ instrumentation. The ISME Journal 6: 513-523.
Yeung, C.-H., C. A. Francis, and C. S. Criddle. 2012. Adaptation of nitrifying microbial biomass to nickel in batch incubations. Applied Microbiology and Biotechnology doi:10.1007/s00253-012-3947-x
Mosier, A. C., E. A. Allen, S. Ferriera, and C. A. Francis. 2012. Genome sequence of "Candidatus Nitrosopumilus salaria" BD31, an ammonia oxidizing archaeon enriched from the San Francisco Bay estuary. J. Bacteriology 194:2119-2120.
Mosier, A. C., E. A. Allen, S. Ferriera, and C. A. Francis. 2012. Genome sequence of a low-salinity ammonia oxidizing archaeon from the San Francisco Bay estuary, "Candidatus Nitrosoarchaeum limnia" BG20. J. Bacteriology 194:2121-2122.
Lund, M., J. M. Smith, and C. A. Francis. 2012. Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea. The ISME Journal doi: 10.1038/ismej.2012.40
Mosier, A.C., M. Lund, and C. A. Francis. 2012. Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microbial Ecology doi: 10.1007/s00248-012-0075-1
Biller, S. J., A. C. Mosier, G. F. Wells, and C. A. Francis. 2012. Global biodiversity of aquatic ammonia-oxidizing archaea is partitioned by habitat. Frontiers in Aquatic Microbiology (in press)
Front Row (left to right) : Chris Francis, Alyson Santoro (currently a Research Assistant Professor, UMCES-Horn Point Laboratory), Samantha Ying, Mike Beman (currently Assistant Professor, UC Merced); Back Row: Colleen Hansel (currently Assistant Professor, Harvard University), Scott Wankel (currently a postdoctoral fellow, Harvard University), Annika Mosier (currently a postdoctoral fellow, UC Berkeley-Banfield Lab), George Wells (currently a postdoctoral fellow, EAWAG, Switzerland). Students and postdocs not shown: Steve Biller (currently a postdoctoral fellow, MIT-Chisholm Lab), Julian Damashek, Jessica Lee, Marie Lund, and Jason Smith.
Last modified Saturday, 07-Jul-2012 12:53:22 PDT
Please contact Chris Francis with questions or comments.