Chris Francis-Home Page- Stanford University

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.

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 Monterey Bay, the central California Current System, 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 acquire novel insights into the ecophysiology of AOA (see our current CSP Projects through the Joint Genome Institute).

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).

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. To fill this knowledge gap, we are using molecular and cultivation-based approaches to characterize the diversity and physiology of Mn(II)-oxidizing bacteria in freshwater, estuarine, and marine environments.

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).

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

2011-present Senior Fellow, Woods Institute for the Environment, 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.

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 6: 1966-1977

Mosier, A.C., M. Lund, and C. A. Francis. 2012. Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microbial Ecology 64: 955-963

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 Microbiologydoi:10.3389/fmicb.2012.00252

Yeung, C.-H., C. A. Francis, and C. S. Criddle. 2013. Adaptation of nitrifying microbial biomass to nickel in batch incubations. Applied Microbiology and Biotechnology 97: 847-857.

Ying, S. C., Y. Masue-Slowey, B. D. Kocar, S. D. Griffis, S. Webb, M. A. Marcus, C. A. Francis, and S. Fendorf. 2013. Distributed microbially- and chemically-mediated redox processes controlling arsenic dynamics within Mn-/Fe-oxide constructed aggregates. Geochimica et Cosmochimica Acta104: 29-41.

Francis, C. A., G. D. O’Mullan, J. C. Cornwell, and B. B. Ward. 2013. Transitions in nirS-type denitrifier diversity, community composition, and biogeochemical activity along the Chesapeake Bay estuary. Frontiers in Aquatic Microbiology doi:10.3389/fmicb.2013.00237

Santoro, A. E., C. M. Sakamoto, J. M. Smith, J. N. Plant, A. L. Gehman, A. Z. Worden, K. S. Johnson, C. A. Francis, and K. L. Casciotti. 2013. Measurements of nitrite production in and around the primary nitrite maximum in the central California Current. Biogeosciences 10: 7395-7410, doi:10.5194/bg-10-7395-2013.

Wells, G. F., Wu, C. H., Piceno, Y. M., Eggleston, B., Brodie, E. L., DeSantis, T. Z., Andersen, G. L., Hazen, T. C., Francis, C. A., Criddle, C. S. 2014. Microbial biogeography across a full-scale wastewater treatment plant transect: evidence for immigration between coupled processes. Applied Microbiology and Biotechnology 98: 4723-4736.

Smith, J.M., K. L. Casciotti, F. P. Chavez, and C. A. Francis. 2014. Differential contributions of archaeal ammonia oxidizer ecotypes to nitrification in coastal surface waters. The ISME Journal 8: 1704-1714.

Smith, J. M., F. P. Chavez, and C. A. Francis. 2014. Ammonium uptake by phytoplankton regulates nitrification in the sunlit ocean. PLoS ONE 9(9): e108173. doi: 10.1371/journal.pone.0108173

Smith, J. M., A. C. Mosier, and C. A. Francis. 2015. Spatiotemporal relationships between the abundance, distribution and potential activities of ammonia-oxidizing and denitrifying microorganisms in intertidal sediments. Microbial Ecology 69: 13-24.

Damashek, J, J. M. Smith, A. C. Mosier, and C. A. Francis. 2015. Benthic ammonia oxidizers differ in community structure and biogeochemical potential across a riverine Delta. Frontiers in Aquatic Microbiology 5: 743 doi: 10.3389/fmicb.2014.00743

Ying, S. C., J. Damashek, S. Fendorf, and C. A. Francis. 2015. Indigenous arsenic(V)-reducing microbial communities in redox fluctuating near-surface sediments of the Mekong Delta. Geobiology 13: 581-587.

Smith, J. M., J. Damashek, F. P. Chavez, and C. A. Francis. 2016. Factors influencing nitrification rates and the abundance and transcriptional activity of ammonia-oxidizing microorganisms in the dark northeast Pacific Ocean. Limnology and Oceanography doi: 10.1002/lno.10235

Damashek, J., K. L. Casciotti, and C. A. Francis. 2016. Variable nitrification rates across environmental gradients in turbid, nutrient-rich estuary waters of San Francisco Bay. Estuaries and Coasts 39: 1050-1071. doi: 10.1007/s12237-016-0071-7.

Lee, J. A., and C. A. Francis. 2017. Spatiotemporal characterization of San Francisco Bay denitrifying communities: a comparison of nirK and nirS diversity and abundance. Microbial Ecology 73(2): 271-284. doi: 10.1007/s00248-016-0865-y

von Sperber, C., O. A. Chadwick, K. L. Casciotti, K. G. Peay, C. A. Francis, A. E. Kim, and P. M. Vitousek. 2017. Controls of nitrogen cycling evaluated along a well-characterized climate gradient. Ecology 98: 1117–1129. doi: 10.1002/ecy.1751

Peay, K., C. von Sperber, E. Cardarelli, H. Toju, C. A. Francis, O. Chadwick, and P. Vitousek. 2017. Convergence and contrast in the community structure of Bacteria, Fungi and Archaea along a tropical elevation-climate gradient. FEMS Microbiology Ecology 93: fix045. doi.org/10.1093/femsec/fix045

Damashek, J., K.P. Pettie, Z.W. Brown, M. M. Mills, K. R. Arrigo, and C. A. Francis. 2017. Regional patterns in ammonia-oxidizing communities throughout Chukchi Sea waters from the Bering Strait to the Beaufort Sea. Aquatic Microbial Ecology 79: 273-286. doi.org/10.3354/ame01834

Tolar, B. B., J. Herrmann, J. R. Bargar, H. van den Bedem, S. Wakatsuki, and C. A. Francis. 2017. Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing Archaea. Environmental Microbiology Reports doi: 10.1111/1758-2229.12567

Damashek, J., and C. A. Francis. 2017. Microbial nitrogen cycling in estuaries: from genes to ecosystem processes. Estuaries and Coasts doi: 10.1007/s12237-017-0306-2

Lee, J. A., and C. A. Francis. 2017. Deep nirS amplicon sequencing of San Francisco Bay sediments enables prediction of geography and environmental conditions from denitrifying community composition. Environmental Microbiology doi: 10.1111/1462-2920.13920

(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 (former PhD student, now postdoc at UGA), Chris Francis, and Linta Reji (PhD student). February 2015. Current students not pictured: Anna Rasmussen (PhD student, started Fall 2016)

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 postdoctoral fellow, UCSB).


	Last modified Monday, 28-Aug-2017 14:26:05 PDT Please contact Chris Francis with questions or comments.