REPORTS the same time [fig. S5A(19) are consistent with chanical invasiveness; and the nanoFETs have high 18. B. 2. Tian, P Xie, T ). Kempa, D. C Bell, C M Lieber, extracellular signals. After a relatively brief (40-s)period of extra- 19. Materials and methods are available as supporting cellular signals, we observed several pronounced References and notes D. A. Giljohann, C.A. Mirkin, Nature 462, 461(2009). 20. C. Conde, A. Caceres, Nat Rev. Neurosci. 10, 319(2009) changes in recorded signals(Fig. 4, B and C, I 2. T. Cohen-Kani, B P. Timko, L. E Weiss, C.M. Lieb . G Leong et al, Proc Not. Acad Sci. USA 106, 703 (2009). and Iln without application of extemal force to Proc. Natl. Acad. Sci. U.S.A. 106, 7309(2009) 22. N Misra et al, Proc. Natl. Acad. Sci. U.S.A. 106, 13780 the PDMS/cell support. Specifically, the initial 3. J. F. Eschermann et al, Appl. Phys. Lett. 95,083703 extracellular signals gradually disappeared(Fig. 4. 0.Qing et al, Proc. Natt. Acad. Sc U.S.A 107, 1882 23. X.]. Zhou, ]. M. Moran-MirabaL, H. G. Craighead, P L McEuen, Nat Nanotechnol. 2, 185(20 4, B and C, Il, pink stars). There was a con- V. Chernomordik, M. M. Kozlov, Nat. Struct. Mol. BioL. comitant decrease in baseline potential, and new 5. 1.Heller, W.T. T Smaal, S.G. Lemay. C.Dekker, Small 5, 15.675(2008) peaks emerged that had an opposite sign, similar 25. w. C Claycomb ef al., Proc. Natl. Acad. Sci. U.S.A 95 6. W. Lu, C M. Lieber, Nat. Mater. 6, 841 (200 2979(1998 requency, much greater amplitude, and longer A Grinvald, R. Hildesheim, Nat. Rev. Neurosci. 5. 874 26. B D Almquist, N A Melosh, Proc. NatL Acad. Sa. USA duration(Fig. 4B, I, green stars). These new 07,5815(2010 peaks, which are coincident with cardiomyocyte 8 M Scanziani, M Hausser, Nature 461, 930(2009) 27.D.M. Bers Nature415,198(2002) 4B, I with an average calibrated peak ampli- 9. We thank G. Yellen, w. C. Claycomb, B. P tude of 80 mv and duration of 200 ms. The E Neher, Anu. Rev. Physiol. 46, 455(1984 amplitude, sign, and duration are near those re-11 Patch Clamping: An Intro Guide to I. Dvir for help with experiments and data analys rted for whole-cell patch clamp recordings from cardiomyocytes(27, 28); thus, we conclude 12. R. M. Wightman, Science 311, 1570(2006). ngineering Faculty Fellow(NSSEFF) award ( N00244-09-1- that these data represent a transition to steady- 13.A G. Ewing, T G Strein, YY Lau, Acc. Chem. Res. 25, 0078), and the McKnight Foundation Neuroscience award. state intracellular recording(Fig. 4A, right) with 0(1992) the 3D nanowire probe 14. M G. Schrlau, N.J.Dun, H H. Bau, ACS Nano 3.563 Supporting Online Material Detailed analysis of the latter steady-state ncemag. org/cgifcontent/full329/5993/830/DC1 eaks(Fig. 4C, I shows five characteristic 15. ]. P. Donoghue, Nat. Neurosci. 5(suppL), 1085 Materials and Methods 2002 of a cardiac intracellular potential (27, 28), M. leong, B. Doris, ]. Kedzierski, K Rim, M. Yang eferences including(a)resting state, (b)rapid depolarization Science306,2057(2004) 10 May 2010: accepted 7 July 2010 (c) plateau, (d) rapid repolarization, and(e) hy- 17. M. Ferrari Nat Rev. Cancer 5, 161(2005) perpolarization. In addition, a sharp transient peak (blue star) and the notch (orange star) possibly associated with the inward sodium and outward potassium currents(28)can be resolved. Optical Terrestrial Gross Carbon dioxide intracellular peaks (ig. SSB)showed the kinked Uptake: Global Distribution and nanowire p region of the cell (19). When the PDMS/cell Covariation with Climate kinked nanowire devices, the intracellular peak disappeared,but they reappeared when the cell Christian Beer, Markus Reichstein, Enrico Tomelleri, Philippe Ciais, Martin Jung, 1 substrate was brought back into gentle contact Nuno Carvalhais 1,3 Christian Rodenbeck, M Altaf Arain, Dennis Baldocchi,6 with the device. This process could be repeated Gordon B Bonan, Alberte Bondeau, Alessandro Cescatti, "Gitta Lasslop, Anders Lindroth.10 multiple times without degradation in the rec- Mark Lomas, Sebastiaan Luyssaert, Hank Margolis, Keith W.oleson, devices were bent into a configuration with angle F lan Woodward,Dario Papale 0<-50o with respect to the substrate, or when kinked nanowire devices were fabricated on Terrestrial gross primary production(GPP)is the largest global CO2 flux driving several ecosystem planar substrates, we could record only extra- functions. We provide an observation-based estimate of this flux at 123+8 petagrams of carbon per cellular signals. These results confirm that elec- year (Pg C year )using eddy covariance flux data and various diagnostic models. Tropical forests and trical recording arises from the highly localized, savannahs account for 60%o. GPP over 40yo of the vegetated land is associated with precipitation pointlike nanoFET near the probe tip, which( State-of-the-art process-oriented biosphere models used for climate predictions exhibit a large tween-model variation of GPPs latitudinal patterns and show higher spatial correlations between imultaneously records both extracellular and GPP and precipitation, suggesting the existence of missing processes or feedback mechanisms which intracellular signals as the nanoFET spans the attenuate the vegetation response to climate. Our estimates of spatially distributed GPP and its cell membrane, and (i)records only intracellular covariation with climate can help improve coupled climate-carbon cycle process models. signals when fully inside the cell. Additional work remains to develop this new restrial plants fix carbon dioxide(co2) the major processes controlling land-atmosphere ynthetic nanoprobe as a routine tool like the as organic compounds through photo- CO2 exchange, providing the capacity of terres- patch-clamp micropipette (10, In), although we synthesis, a carbon (C) flux also known trial ecosystems to partly offset anthropogenic believe that there are already clear advantages: at the ecosystem level as gross primary produc- CO2 emissions. Electrical recording with kinked nanowire tion(GPP). Terrestrial GPP is the largest global Although photosynthesis at the leaf and can- probes is relatively simple without the need for carbon flux, and it drives several ecosystem func- opy level are quite well understood, only tentative resistance or capacitance compensation (9, In): tions, such as respiration and growth GPP thus observation-based estimates of global terrestrial the nanoprobes are chemically less invasive than contributes to human welfare because it is the GPP have been possible so far. Plant- and stand- pipettes, as there is no solution exchange, the basis for food, fiber, and wood production. In level GPP has previously been calculated as two small size and biomimetic coating minimizes me- addition, GPP, along with respiration, is one of times biomass production(1, 2), with substantial 834 13AuguSt2010Vol329ScieNcewww.sciencemag.orgthe same time [fig. S5A (19)] are consistent with extracellular signals. After a relatively brief (~40-s) period of extra￾cellular signals, we observed several pronounced changes in recorded signals (Fig. 4, B and C, II and III) without application of external force to the PDMS/cell support. Specifically, the initial extracellular signals gradually disappeared (Fig. 4, B and C, II, pink stars). There was a con￾comitant decrease in baseline potential, and new peaks emerged that had an opposite sign, similar frequency, much greater amplitude, and longer duration (Fig. 4B, II, green stars). These new peaks, which are coincident with cardiomyocyte cell beating, rapidly reached a steady state (Fig. 4B, III) with an average calibrated peak ampli￾tude of ~80 mV and duration of ~200 ms. The amplitude, sign, and duration are near those re￾ported for whole-cell patch clamp recordings from cardiomyocytes (27, 28); thus, we conclude that these data represent a transition to steady￾state intracellular recording (Fig. 4A, right) with the 3D nanowire probe. Detailed analysis of the latter steady-state peaks (Fig. 4C, III) shows five characteristic phases of a cardiac intracellular potential (27, 28), including (a) resting state, (b) rapid depolarization, (c) plateau, (d) rapid repolarization, and (e) hy￾perpolarization. In addition, a sharp transient peak (blue star) and the notch (orange star) possibly associated with the inward sodium and outward potassium currents (28) can be resolved. Optical images recorded at the same time as these intracellular peaks (fig. S5B) showed the kinked nanowire probe tips in a possible intracellular region of the cell (19). When the PDMS/cell substrate was mechanically retracted from the 3D kinked nanowire devices, the intracellular peaks disappeared, but they reappeared when the cell substrate was brought back into gentle contact with the device. This process could be repeated multiple times without degradation in the rec￾orded signal. When vertical 3D nanoprobe devices were bent into a configuration with angle q < ~50° with respect to the substrate, or when kinked nanowire devices were fabricated on planar substrates, we could record only extra￾cellular signals. These results confirm that elec￾trical recording arises from the highly localized, pointlike nanoFET near the probe tip, which (i) initially records only extracellular potential, (ii) simultaneously records both extracellular and intracellular signals as the nanoFET spans the cell membrane, and (iii) records only intracellular signals when fully inside the cell. Additional work remains to develop this new synthetic nanoprobe as a routine tool like the patch-clamp micropipette (10, 11), although we believe that there are already clear advantages: Electrical recording with kinked nanowire probes is relatively simple without the need for resistance or capacitance compensation (9, 11); the nanoprobes are chemically less invasive than pipettes, as there is no solution exchange; the small size and biomimetic coating minimizes me￾chanical invasiveness; and the nanoFETs have high spatial and temporal resolution for recording. References and Notes 1. D. A. Giljohann, C. A. Mirkin, Nature 462, 461 (2009). 2. T. Cohen-Karni, B. P. Timko, L. E. Weiss, C. M. Lieber, Proc. Natl. Acad. Sci. U.S.A. 106, 7309 (2009). 3. J. F. Eschermann et al., Appl. Phys. Lett. 95, 083703 (2009). 4. Q. Qing et al., Proc. Natl. Acad. Sci. U.S.A. 107, 1882 (2010). 5. I. Heller, W. T. T. Smaal, S. G. Lemay, C. Dekker, Small 5, 2528 (2009). 6. W. Lu, C. M. Lieber, Nat. Mater. 6, 841 (2007). 7. A. Grinvald, R. Hildesheim, Nat. Rev. Neurosci. 5, 874 (2004). 8. M. Scanziani, M. Häusser, Nature 461, 930 (2009). 9. R. D. Purves, Microelectrode Methods for Intracellular Recording and Ionophoresis (Academic Press, London, 1981). 10. B. Sakmann, E. Neher, Annu. Rev. Physiol. 46, 455 (1984). 11. A. Molleman, Patch Clamping: An Introductory Guide to Patch Clamp Electrophysiology (Wiley, Chichester, UK, 2003). 12. R. M. Wightman, Science 311, 1570 (2006). 13. A. G. Ewing, T. G. Strein, Y. Y. Lau, Acc. Chem. Res. 25, 440 (1992). 14. M. G. Schrlau, N. J. Dun, H. H. Bau, ACS Nano 3, 563 (2009). 15. J. P. Donoghue, Nat. Neurosci. 5 (suppl.), 1085 (2002). 16. M. Ieong, B. Doris, J. Kedzierski, K. Rim, M. Yang, Science 306, 2057 (2004). 17. M. Ferrari, Nat. Rev. Cancer 5, 161 (2005). 18. B. Z. Tian, P. Xie, T. J. Kempa, D. C. Bell, C. M. Lieber, Nat. Nanotechnol. 4, 824 (2009). 19. Materials and methods are available as supporting material on Science Online. 20. C. Conde, A. Cáceres, Nat. Rev. Neurosci. 10, 319 (2009). 21. T. G. Leong et al., Proc. Natl. Acad. Sci. U.S.A. 106, 703 (2009). 22. N. Misra et al., Proc. Natl. Acad. Sci. U.S.A. 106, 13780 (2009). 23. X. J. Zhou, J. M. Moran-Mirabal, H. G. Craighead, P. L. McEuen, Nat. Nanotechnol. 2, 185 (2007). 24. L. V. Chernomordik, M. M. Kozlov, Nat. Struct. Mol. Biol. 15, 675 (2008). 25. W. C. Claycomb et al., Proc. Natl. Acad. Sci. U.S.A. 95, 2979 (1998). 26. B. D. Almquist, N. A. Melosh, Proc. Natl. Acad. Sci. U.S.A. 107, 5815 (2010). 27. D. M. Bers, Nature 415, 198 (2002). 28. D. P. Zipes, J. Jalife, Cardiac Electrophysiology: From Cell to Bedside (Saunders, Philadelphia, ed. 2, 2009). 29. We thank G. Yellen, W. C. Claycomb, B. P. Bean, P. T. Ellinor, G. H. Yu, D. Casanova, B. P. Timko, and T. Dvir for help with experiments and data analysis. C.M.L. acknowledges support from a NIH Director’s Pioneer Award (5DP1OD003900), a National Security Science and Engineering Faculty Fellow (NSSEFF) award (N00244-09-1- 0078), and the McKnight Foundation Neuroscience award. Supporting Online Material www.sciencemag.org/cgi/content/full/329/5993/830/DC1 Materials and Methods Figs. S1 to S5 References 10 May 2010; accepted 7 July 2010 10.1126/science.1192033 Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate Christian Beer,1 * Markus Reichstein,1 Enrico Tomelleri,1 Philippe Ciais,2 Martin Jung,1 Nuno Carvalhais,1,3 Christian Rödenbeck,4 M. Altaf Arain,5 Dennis Baldocchi,6 Gordon B. Bonan,7 Alberte Bondeau,8 Alessandro Cescatti,9 Gitta Lasslop,1 Anders Lindroth,10 Mark Lomas,11 Sebastiaan Luyssaert,12 Hank Margolis,13 Keith W. Oleson,7 Olivier Roupsard,14,15 Elmar Veenendaal,16 Nicolas Viovy,2 Christopher Williams,17 F. Ian Woodward,11 Dario Papale18 Terrestrial gross primary production (GPP) is the largest global CO2 flux driving several ecosystem functions. We provide an observation-based estimate of this flux at 123 T 8 petagrams of carbon per year (Pg C year−1 ) using eddy covariance flux data and various diagnostic models. Tropical forests and savannahs account for 60%. GPP over 40% of the vegetated land is associated with precipitation. State-of-the-art process-oriented biosphere models used for climate predictions exhibit a large between-model variation of GPP’s latitudinal patterns and show higher spatial correlations between GPP and precipitation, suggesting the existence of missing processes or feedback mechanisms which attenuate the vegetation response to climate. Our estimates of spatially distributed GPP and its covariation with climate can help improve coupled climate–carbon cycle process models. Terrestrial plants fix carbon dioxide (CO2) as organic compounds through photo￾synthesis, a carbon (C) flux also known at the ecosystem level as gross primary produc￾tion (GPP). Terrestrial GPP is the largest global carbon flux, and it drives several ecosystem func￾tions, such as respiration and growth. GPP thus contributes to human welfare because it is the basis for food, fiber, and wood production. In addition, GPP, along with respiration, is one of the major processes controlling land-atmosphere CO2 exchange, providing the capacity of terres￾trial ecosystems to partly offset anthropogenic CO2 emissions. Although photosynthesis at the leaf and can￾opy level are quite well understood, only tentative observation-based estimates of global terrestrial GPP have been possible so far. Plant- and stand￾level GPP has previously been calculated as two times biomass production (1, 2), with substantial 834 13 AUGUST 2010 VOL 329 SCIENCE www.sciencemag.org REPORTS