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Sulfur Oxidation Genes in Diverse Deep-Sea Viruses
Virus-Enhanced Sulfur Oxidation
How do microbial viruses affect subsurface microbial communities? Anantharaman et al. (p. 757, published online 1 May) investigated the interactions between ubiquitous marine lithotrophs found at hydrothermal vents and their viruses. The genes for sulfur oxidation in viruses that infect abundant marine chemosynthetic sulfur-oxidizing bacteria enhanced sulfur oxidation, thereby influencing the biogeochemical sulfur cycle.
Abstract
Viruses are the most abundant biological entities in the oceans and a pervasive cause of mortality of microorganisms that drive biogeochemical cycles. Although the ecological and evolutionary effects of viruses on marine phototrophs are well recognized, little is known about their impact on ubiquitous marine lithotrophs. Here, we report 18 genome sequences of double-stranded DNA viruses that putatively infect widespread sulfur-oxidizing bacteria. Fifteen of these viral genomes contain auxiliary metabolic genes for the α and γ subunits of reverse dissimilatory sulfite reductase (rdsr). This enzyme oxidizes elemental sulfur, which is abundant in the hydrothermal plumes studied here. Our findings implicate viruses as a key agent in the sulfur cycle and as a reservoir of genetic diversity for bacterial enzymes that underpin chemosynthesis in the deep oceans.
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1
Swan B. K., Martinez-Garcia M., Preston C. M., Sczyrba A., Woyke T., Lamy D., Reinthaler T., Poulton N. J., Masland E. D., Gomez M. L., Sieracki M. E., DeLong E. F., Herndl G. J., Stepanauskas R., Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333, 1296–1300 (2011).
2
Arístegui J., Gasol J. M., Duarte C. M., Herndl G. J., Microbial oceanography of the dark ocean’s pelagic realm. Limnol. Oceanogr. 54, 1501–1529 (2009).
3
Reinthaler T., van Aken H. M., Herndl G. J., Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic’s interior. Deep-Sea Res. II 57, 1572–1580 (2010).
4
Anantharaman K., Breier J. A., Sheik C. S., Dick G. J., Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc. Natl. Acad. Sci. U.S.A. 110, 330–335 (2013).
5
Newton I. L., Woyke T., Auchtung T. A., Dilly G. F., Dutton R. J., Fisher M. C., Fontanez K. M., Lau E., Stewart F. J., Richardson P. M., Barry K. W., Saunders E., Detter J. C., Wu D., Eisen J. A., Cavanaugh C. M., The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315, 998–1000 (2007).
6
Petersen J. M., Zielinski F. U., Pape T., Seifert R., Moraru C., Amann R., Hourdez S., Girguis P. R., Wankel S. D., Barbe V., Pelletier E., Fink D., Borowski C., Bach W., Dubilier N., Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476, 176–180 (2011).
7
Walsh D. A., Zaikova E., Howes C. G., Song Y. C., Wright J. J., Tringe S. G., Tortell P. D., Hallam S. J., Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science 326, 578–582 (2009).
8
Canfield D. E., Stewart F. J., Thamdrup B., De Brabandere L., Dalsgaard T., Delong E. F., Revsbech N. P., Ulloa O., A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science 330, 1375–1378 (2010).
9
Hara S., Koike I., Terauchi K., Kamiya H., Tanoue E., Abundance of viruses in deep oceanic waters. Mar. Ecol. Prog. Ser. 145, 269–277 (1996).
10
Dick G. J., Tebo B. M., Microbial diversity and biogeochemistry of the Guaymas Basin deep-sea hydrothermal plume. Environ. Microbiol. 12, 1334–1347 (2010).
11
Lesniewski R. A., Jain S., Anantharaman K., Schloss P. D., Dick G. J., The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs. ISME J. 6, 2257–2268 (2012).
12
Dick G. J., Andersson A. F., Baker B. J., Simmons S. L., Thomas B. C., Yelton A. P., Banfield J. F., Community-wide analysis of microbial genome sequence signatures. Genome Biol. 10, R85 (2009).
13
Casjens S. R., Gilcrease E. B., Winn-Stapley D. A., Schicklmaier P., Schmieger H., Pedulla M. L., Ford M. E., Houtz J. M., Hatfull G. F., Hendrix R. W., The generalized transducing Salmonella bacteriophage ES18: Complete genome sequence and DNA packaging strategy. J. Bacteriol. 187, 1091–1104 (2005).
14
Sheik C. S., Jain S., Dick G. J., Metabolic flexibility of enigmatic SAR324 revealed through metagenomics and metatranscriptomics. Environ. Microbiol. 16, 304–317 (2014).
15
Breitbart M., Thompson L. R., Suttle C. A., Sullivan M. B., Exploring the vast diversity of marine viruses. Oceanography 20, 135–139 (2007).
16
Breitbart M., Marine viruses: Truth or dare. Annu. Rev. Mar. Sci. 4, 425–448 (2012).
17
Ignacio-Espinoza J. C., Sullivan M. B., Phylogenomics of T4 cyanophages: Lateral gene transfer in the “core” and origins of host genes. Environ. Microbiol. 14, 2113–2126 (2012).
18
Lindell D., Sullivan M. B., Johnson Z. I., Tolonen A. C., Rohwer F., Chisholm S. W., Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl. Acad. Sci. U.S.A. 101, 11013–11018 (2004).
19
Ghosh W., Dam B., Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol. Rev. 33, 999–1043 (2009).
20
Hensen D., Sperling D., Trüper H. G., Brune D. C., Dahl C., Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol. Microbiol. 62, 794–810 (2006).
21
Marshall K. T., Morris R. M., Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic96BD-19 clade. ISME J. 7, 452–455 (2013).
22
Lindell D., Jaffe J. D., Johnson Z. I., Church G. M., Chisholm S. W., Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89 (2005).
23
Materials and methods are available as supplementary materials on Science Online.
24
McCollom T. M., Geochemical constraints on primary productivity in submarine hydrothermal vent plumes. Deep-Sea Res. I 47, 85–101 (2000).
25
Breier J. A., Toner B. M., Fakra S. C., Marcus M. A., White S. N., Thurnherr A. M., German C. R., Sulfur, sulfides, oxides and organic matter aggregated in submarine hydrothermal plumes at 9°50′N East Pacific Rise. Geochim. Cosmochim. Acta 88, 216–236 (2012).
26
Li M., Toner B. M., Baker B. J., Breier J. A., Sheik C. S., Dick G. J., Microbial iron uptake as a mechanism for dispersing iron from deep-sea hydrothermal vents. Nat. Commun. 5, 3192 (2014).
27
Avrani S., Wurtzel O., Sharon I., Sorek R., Lindell D., Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474, 604–608 (2011).
28
Hurwitz B. L., Sullivan M. B., The Pacific Ocean virome (POV): A marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLOS ONE 8, e57355 (2013).
29
Klein M., Friedrich M., Roger A. J., Hugenholtz P., Fishbain S., Abicht H., Blackall L. L., Stahl D. A., Wagner M., Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J. Bacteriol. 183, 6028–6035 (2001).
30
Breier J. A., Rauch C. G., McCartney K., Toner B. M., Fakra S. C., White S. N., German C. R., A suspended-particle rosette multi-sampler for discrete biogeochemical sampling in low-particle-density waters. Deep-Sea Res. I 56, 1579–1589 (2009).
31
Peng Y., Leung H. C. M., Yiu S. M., Chin F. Y. L., IDBA-UD: A de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428 (2012).
32
Zerbino D. R., Birney E., Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829 (2008).
33
Namiki T., Hachiya T., Tanaka H., Sakakibara Y., MetaVelvet: An extension of Velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res. 40, e155 (2012).
34
Schmieder R., Lim Y. W., Edwards R., Identification and removal of ribosomal RNA sequences from metatranscriptomes. Bioinformatics 28, 433–435 (2012).
35
Markowitz V. M., Ivanova N. N., Szeto E., Palaniappan K., Chu K., Dalevi D., Chen I. M., Grechkin Y., Dubchak I., Anderson I., Lykidis A., Mavromatis K., Hugenholtz P., Kyrpides N. C., IMG/M: A data management and analysis system for metagenomes. Nucleic Acids Res. 36 (suppl. 1), D534–D538 (2008).
36
Hyatt D., Chen G. L., Locascio P. F., Land M. L., Larimer F. W., Hauser L. J., Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).
37
Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J., Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
38
Quevillon E., Silventoinen V., Pillai S., Harte N., Mulder N., Apweiler R., Lopez R., InterProScan: Protein domains identifier. Nucleic Acids Res. 33 (suppl. 2), W116–W120 (2005).
39
Zhao Y., Temperton B., Thrash J. C., Schwalbach M. S., Vergin K. L., Landry Z. C., Ellisman M., Deerinck T., Sullivan M. B., Giovannoni S. J., Abundant SAR11 viruses in the ocean. Nature 494, 357–360 (2013).
40
Sullivan M. B., Huang K. H., Ignacio-Espinoza J. C., Berlin A. M., Kelly L., Weigele P. R., DeFrancesco A. S., Kern S. E., Thompson L. R., Young S., Yandava C., Fu R., Krastins B., Chase M., Sarracino D., Osburne M. S., Henn M. R., Chisholm S. W., Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ. Microbiol. 12, 3035–3056 (2010).
41
Šimoliūnas E., Kaliniene L., Truncaitė L., Zajančkauskaitė A., Staniulis J., Kaupinis A., Ger M., Valius M., Meškys R., Klebsiella phage vB_KleM-RaK2—A giant singleton virus of the family Myoviridae. PLOS ONE 8, e60717 (2013).
42
Krzywinski M., Schein J., Birol I., Connors J., Gascoyne R., Horsman D., Jones S. J., Marra M. A., Circos: An information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009).
43
Edgar R. C., MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
44
Karkhoff-Schweizer R. R., Huber D. P., Voordouw G., Conservation of the genes for dissimilatory sulfite reductase from Desulfovibrio vulgaris and Archaeoglobus fulgidus allows their detection by PCR. Appl. Environ. Microbiol. 61, 290–296 (1995).
45
Weissgerber T., Zigann R., Bruce D., Chang Y. J., Detter J. C., Han C., Hauser L., Jeffries C. D., Land M., Munk A. C., Tapia R., Dahl C., Complete genome sequence of Allochromatium vinosum DSM 180T. Stand. Genomic Sci. 5, 311–330 (2011).
46
Dahl C., Kredich N. M., Deutzmann R., Trüper H. G., Dissimilatory sulphite reductase from Archaeoglobus fulgidus: Physico-chemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes. J. Gen. Microbiol. 139, 1817–1828 (1993).
47
Dhillon A., Goswami S., Riley M., Teske A., Sogin M., Domain evolution and functional diversification of sulfite reductases. Astrobiology 5, 18–29 (2005).
48
Oliveira T. F., Vonrhein C., Matias P. M., Venceslau S. S., Pereira I. A., Archer M., The crystal structure of Desulfovibrio vulgaris dissimilatory sulfite reductase bound to DsrC provides novel insights into the mechanism of sulfate respiration. J. Biol. Chem. 283, 34141–34149 (2008).
49
Stamatakis A., RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).
50
Duhaime M. B., Wichels A., Waldmann J., Teeling H., Glöckner F. O., Ecogenomics and genome landscapes of marine Pseudoalteromonas phage H105/1. ISME J. 5, 107–121 (2011).
51
Mottl M. J., Seewald J. S., Wheat C. G., Tivey M. K., Michael P. J., Proskurowski G., McCollom T. M., Reeves E., Sharkey J., You C.-F., Chan L.-H., Pichler T., Chemistry of hot springs along the Eastern Lau Spreading Center. Geochim. Cosmochim. Acta 75, 1013–1038 (2011).
52
Bowers T. S., Von Damm K. L., Edmond J. M., Chemical evolution of mid-ocean ridge hot springs. Geochim. Cosmochim. Acta 49, 2239–2252 (1985).
53
Janecky D. R., Seyfried W. E., Formation of massive sulfide deposits on oceanic ridge crests: Incremental reaction models for mixing between hydrothermal solutions and seawater. Geochim. Cosmochim. Acta 48, 2723–2738 (1984).
54
J. Seewald, T. McCollom, G. Proskurowski, E. Reeves, M. Mottl, J. Sharkey, C. G. Wheat, M. Tivey, “Aqueous volatiles in Lau Basin hydrothermal fluids.” in AGU Fall Meeting Abstracts (American Geophysical Union, Washington, DC, 2005), vol. 1, p. 0478.
55
Brandes J. A., Boctor N. Z., Cody G. D., Cooper B. A., Hazen R. M., Yoder H. S., Abiotic nitrogen reduction on the early Earth. Nature 395, 365–367 (1998).
56
L. D. Talley, Ed., Hydrographic Atlas of the World Ocean Circulation Experiment (WOCE) (International WOCE Project Office, Southampton, UK, 2007).
57
Conrad R., Seiler W., Methane and hydrogen in seawater (Atlantic Ocean). Deep-Sea Res. I 35, 1903–1917 (1988).
58
Weiss R. F., Craig H., Precise shipboard determination of dissolved nitrogen, oxygen, argon, and total inorganic carbon by gas chromatography. Deep-Sea Res. Oceanogr. Abstr. 20, 291–303 (1973).
59
Johnson J. W., Oelkers E. H., Helgeson H. C., SUPCRT92: A software package for calculating the standard molal thermodynamic properties of minerals, gases, aqueous species, and reactions from 1 to 5000 bar and 0 to 1000°C. Comput. Geosci. 18, 899–947 (1992).
60
Helgeson H. C., Delaney J. M., Nesbitt H. W., Bird D. K., Summary and critique of the thermodynamic properties of rock-forming minerals. Am. J. Sci. 278-A, 1–229 (1978).
61
McCollom T. M., Shock E. L., Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim. Cosmochim. Acta 61, 4375–4391 (1997).
62
Saccocia P. J., Seyfried W. E., The solubility of chlorite solid solutions in 3.2 wt% NaCl fluids from 300–400°C, 500 bars. Geochim. Cosmochim. Acta 58, 567–585 (1994).
63
Shock E. L., Helgeson H. C., Calculation of the thermodynamic and transport properties of aqueous species at high pressures and temperatures: Correlation algorithms for ionic species and equation of state predictions to 5 kb and 1000°C. Geochim. Cosmochim. Acta 52, 2009–2036 (1988).
64
Shock E. L., Helgeson H. C., Sverjensky D. A., Calculation of the thermodynamic and transport properties of aqueous species at high pressures and temperatures: Standard partial molal properties of inorganic neutral species. Geochim. Cosmochim. Acta 53, 2157–2183 (1989).
65
Shock E. L., Sassani D. C., Willis M., Sverjensky D. A., Inorganic species in geologic fluids: Correlations among standard molal thermodynamic properties of aqueous ions and hydroxide complexes. Geochim. Cosmochim. Acta 61, 907–950 (1997).
66
Sverjensky D. A., Shock E. L., Helgeson H. C., Prediction of the thermodynamic properties of aqueous metal complexes to 1000°C and 5 kb. Geochim. Cosmochim. Acta 61, 1359–1412 (1997).
67
R. A. Robie, B. S. Hemingway, J. R. Fisher, in Thermodynamic Properties of Minerals and Related Substances at 298.15 K and 1 Bar (10 Pascals) Pressure and at Higher Temperatures. Bulletin 1452 (U.S. Geological Survey, Reston, VA, 1979), pp. 456.
68
Wagman D. D., Evans W. H., Parker V. B., Schumm R. H., Halow I., Bailey S. M., Churney K. L., Nuttall R. L., The NBS tables of chemical thermodynamic properties: Selected values for inorganic and C1 and C2 organic substances in SI units. J. Phys. Chem. Ref. Data 11 (suppl. 2), 1–392 (1982).
69
Helgeson H. C., Thermodynamics of hydrothermal systems at elevated temperatures and pressures. Am. J. Sci. 267, 729–804 (1969).
70
Helgeson H. C., Kirkham D. H., Theoretical prediction of the thermodynamic behavior of aqueous electrolytes at high pressures and temperatures; II, Debye-Huckel parameters for activity coefficients and relative partial molal properties. Am. J. Sci. 274, 1199–1261 (1974).
71
C. M. Bethke, Geochemical and Biogeochemical Reaction Modeling (Cambridge Univ. Press, Cambridge, ed. 2, 2007).
72
Cleverley J. S., Bastrakov E. N., K2GWB: Utility for generating thermodynamic data files for The Geochemist’s Workbench® at 0–1000°C and 1–5000bar from UT2K and the UNITHERM database. Comput. Geosci. 31, 756–767 (2005).
73
S. E. Drummond, thesis, Pennsylvania State University (1981).
74
Marcus M. A., MacDowell A. A., Celestre R., Manceau A., Miller T., Padmore H. A., Sublett R. E., Beamline 10.3.2 at ALS: A hard x-ray microprobe for environmental and materials sciences. J. Synchrotron Radiat. 11, 239–247 (2004).
75
Hammersley A. P., Svensson S. O., Hanfland M., Fitch A. N., Hausermann D., Two-dimensional detector software: From real detector to idealised image or two-theta scan. High Press. Res. 14, 235–248 (1996).
76
Sangal V., Fineran P. C., Hoskisson P. A., Novel configurations of type I and II CRISPR-Cas systems in Corynebacterium diphtheriae. Microbiology 159, 2118–2126 (2013).
77
Hurwitz B. L., Hallam S. J., Sullivan M. B., Metabolic reprogramming by viruses in the sunlit and dark ocean. Genome Biol. 14, R123 (2013).
78
Von Damm K. L., Edmond J. M., Measures C. I., Grant B., Chemistry of submarine hydrothermal solutions at Guaymas Basin, Gulf of California. Geochim. Cosmochim. Acta 49, 2221–2237 (1985).
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Volume 344 | Issue 6185
16 May 2014
16 May 2014
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Received: 14 February 2014
Accepted: 16 April 2014
Published in print: 16 May 2014
Acknowledgments
This project is funded in part by the Gordon and Betty Moore Foundation (grant GBMF2609) and the NSF (grants OCE1038006, OCE1038055, OCE1037991, and OCE1029242). We thank the University of Michigan Rackham Graduate School Faculty Research Fellowship Program for their support and M. Li and S. Jain for their assistance. DNA sequencing was conducted at the University of Michigan DNA Sequencing Core. We acknowledge the captain and crew of R/V Thomas G. Thompson, Chief Scientist A.-L. Reysenbach, and J. Sylvan for sampling and logistical support. For assistance with synchrotron measurements at BL10.3.2, we thank K. J. Edwards, J. V. Sorensen, M. A. Marcus, and S. C. Fakra. The Advanced Light Source is supported by the Director, Office of Science, Office of Basic Energy Sciences, of the U.S. Department of Energy (DOE) under contract no. DE-AC02-05CH11231. The nucleotide sequences are available from DOE JGI-IMG/MER (Taxon Object IDs: Kilo Moana, 3300001680; ABE, 3300001681; Mariner, 3300001678; Tahi Moana, 3300001679; Tui Malila, 3300001676; Guaymas, 3300001683) and the National Center for Biotechnology Information (BioProject: PRJNA234377). We declare no competing financial interests.
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