A Biomarker Based on the Stable Isotopes of Nickel
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A biomarker based on the stable isotopes of nickel Vyllinniskii Camerona,b,1, Derek Vanceb, Corey Archerb, and Christopher H. Housea aDepartment of Geosciences and Penn State Astrobiology Research Center, The Pennsylvania State University, University Park, PA 16802; and bBristol Isotope Group, Department of Earth Sciences, University of Bristol, Bristol BS8 1RJ, United Kingdom Edited by Donald E. Canfield, University of Southern Denmark, Odense M., Denmark, and approved May 20, 2009 (received for review January 22, 2009) The new stable isotope systems of transition metals are increas- this may be more true for some trace metal isotope systems than ingly used to understand and quantify the impact of primitive others. microbial metabolisms on the modern and ancient Earth. To date, Of key importance to our study is nickel’s role as a bioessential little effort has been expended on nickel (Ni) isotopes but there are trace metal. Microorganisms use trace metals typically as mi- good reasons to believe that this system may be more straight- cronutrients, notably for vital roles in enzymes, and the amounts forward, and useful in this respect, than some others. Here, we needed are analogous to the metal concentration in seawater present Ni stable isotope data for abiotic terrestrial samples and (22). At least 3 of the 7 known Ni enzymes are found in pure cultures of methanogens. The dataset for rocks reveals little methanogens (23) and only one, urease, is used by higher-order isotopic variability and provides a lithologic baseline for terrestrial Ni organisms in nitrogen metabolism (22). From a functional and isotope studies. In contrast, methanogens assimilate the light iso- evolutionary perspective, the absolute requirement for Ni by topes, yielding residual media with a complementary heavy isotopic methanogens and particularly by one very special enzyme, enrichment. Methanogenesis may have evolved during or before the methyl-coenzyme M reductase (MCR), exemplifies what could Archean, when methane could have been key to Earth’s early sys- be termed a class-specific metal dependency. Briefly, methano- tems. Our data suggest significant potential in Ni stable isotopes for genesis is the process by which methanogens generate energy via identifying and quantifying methanogenesis on the early planet. a stepwise reduction of single-carbon substrates; concomitantly, Additionally, Ni stable isotope fractionation may well prove to be the methane is produced as a waste product. The terminal process fundamental unambiguous trace metal biomarker for methanogens. of methane formation involves MCR whose active site is a unique Ni cofactor, F430, which is found only in methanogens and biological fractionation ͉ early life ͉ methanogens ͉ trace metal whose only known function is the catalytic activity within MCR (23–25). An analogue of MCR that catalyzes reverse methano- ife has had a profound impact on the surface of the Earth, genesis, the anaerobic oxidation of methane (AOM), has been Lwith perhaps the most obvious expression being the advent of proposed (26), but its identity, structure and function remain oxygenic photosynthesis leading to the evolution of an oxidised unknown. Another intriguing Ni enzyme is the bifunctional atmosphere and oceans (1, 2). However, the microorganisms and CODH/ACS cluster; microorganisms possessing these enzymes metabolisms mediating oxygenic photosynthesis probably use the Wood-Ljungdahl pathway for growth and are thought to evolved relatively late in the Archean (3–5) and other metabo- be evolutionarily primitive. Several lines of support for this lisms, such as methanogenesis, likely dominated both the early concept are described in refs. 27 and 28. history of the biosphere itself (6–8) and the surface chemistry of Here, we present the first Ni isotope data for abiotic terrestrial the planet (9, 10). For example, atmospheric methane has been samples, for pure cultures of laboratory-grown methanogens and suggested as the dominant greenhouse gas before 2.3 Ga, before for cultures of one heterotrophic Archaea. Nickel is a first row the evolution of oxic conditions (10). This inference is based on transition metal. Although it can occupy a range of oxidation ϩ ϩ models of solar luminosity, atmospheric photochemistry and states from 0 to 4 , the 2 state is essentially the only natural Archean microbial ecology, but little is known about the actual oxidation state. This makes for a key difference from the Fe timing of the evolution of methanogens or methanogenesis as a system. To date, Ni isotope studies have focused almost exclu- sively on extraterrestrial materials and the search for radiogenic metabolism. Phylogenetic studies indicate methanogens are deeply 60 60 rooted in the tree of life (6, 8, 11), but this approach relies on Ni, the decay product of extinct Fe (29–33). Within analytical biological evidence to constrain the timing of evolutionary events. uncertainties, these studies have demonstrated a fairly homog- In the investigation of the history of life on Earth, isotopic and enous Ni isotopic composition for the early solar system, al- chemical biomarkers serve both to calibrate time in phylogenetic though 2 studies report moderate stable isotope variability for trees and to document the impact of the biosphere on the specific meteoritic fractions (30, 32). In the modern oceans, Ni distributions are dominated by scavenging and the element has physical world. An array of tools has traditionally been har- Ϸ nessed, including organic molecules (12) and the isotopic com- an oceanic residence time of 10,000 years (34). position of key bioactive elements whose surface geochemical Results cycles are dominated by the biosphere (13). The transition metals are a recent addition to the latter group, with Fe Our new Ni stable isotope data, along with details of the undergoing the most intensive study (14, 15). Fe has advantages experimental and analytical methods, are presented in the SI and disadvantages in this regard, as the many studies conducted Text and summarized in Fig. 1. The first observation is that key on its isotope system have shown. The ubiquitous role of Fe in abiotic terrestrial samples, representing the mantle and crust, the biosphere makes its isotopes a key system to study, though show very little variation in Ni isotopic composition (Fig. 1A: other isotope systems such as Se (16) and Cu (17) may also be promising. A substantial body of work (for example, see refs. 15 Author contributions: V.C. and C.H.H. designed research; V.C. performed research; V.C., and 18–21) has documented the various issues characterizing the D.V., and C.A. contributed new reagents/analytic tools; V.C. and D.V. analyzed data; and interpretation of isotopic fractionations of virtually every iso- V.C. and D.V. wrote the paper. tope system that has been developed. For example, transitions The authors declare no conflict of interest. between oxidation states can impart fractionations that may be This article is a PNAS Direct Submission. attributable to any number of abiological processes and biological 1To whom correspondence should be addressed. E-mail: [email protected]. vital effects. Pinpointing isotopic fractionations directly ascribed to This article contains supporting information online at www.pnas.org/cgi/content/full/ the latter has not been shown to be a particularly easy task although 0900726106/DCSupplemental. 10944–10948 ͉ PNAS ͉ July 7, 2009 ͉ vol. 106 ͉ no. 27 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0900726106 Downloaded by guest on September 29, 2021 relative to the starting media and Ni was fractionated irrespective of phylogenetic differences. Many of the experiments resulted in no significant Ni depletions in the medium (i.e., no reservoir effect) so that the measured cell ␦60Ni yields a direct estimate of the fractionation of Ni isotopes into methanogen cells. As shown in Fig. 1B, cells of M. barkeri harvested from 2 separate experiments yielded values that are different from the starting medium 60 (⌬␦ Nicells-starting medium) to an identical degree (Ϫ0.83 Ϯ 0.09 and Ϫ0.86 Ϯ 0.09‰), whereas a third experiment (experiment 2) had a smaller fractionation but larger uncertainty (Ϫ0.44 Ϯ 0.20). Two 60 of 5 M. acetivorans experiments yielded ⌬␦ Nicells-starting medium of Ϫ0.63 and Ϫ0.84. Two of the five M. jannaschii experiments yielded analytically identical values of Ϫ0.96 Ϯ 0.09 and Ϫ0.81 Ϯ 0.06, whereas the third gave a large fractionation of Ϫ1.46 Ϯ 0.08. In a few experiments (e.g., M. acetivorans experiment 2) sub- stantial proportions of the total starting Ni in the system is contained within the cells, and as a result the residual media are, as expected from mass balance, significantly heavier than the starting Ni. The results, along with the data for all experiments where the total Ni mass balance is also available, are presented in Fig. 2. The Ni uptake experiment (Fig. 3) conducted with M. acetivorans was specifically designed to monitor the isotopic evolution of the residual medium as cells grow, removing and sequestering more Ni from the system. Cells were harvested only once at the end of this experiment and during the exponential phase of growth. For this terminal stage of the experiment, the amount of Ni taken up into cells (1.2 g) represents Ϸ25% of total originally available Ni. The data for the final cells, and all but one of the analyses of the evolving Fig. 1. Nickel stable isotope data for meteorites, terrestrial basalts and residual media, fit reasonably well to a closed-system Rayleigh sediments (A) and cultures of Archaea (B) plotted on the same vertical scale. model with an alpha [(60Ni/58Ni) /(60Ni/58Ni) ] ϭϷ0.9990– For the meteorite data in A, filled symbols are for stones and open symbols for cells medium 0.9993 [i.e., cellular Ni Ϫ1.0 to Ϫ0.7‰ relative to medium, where irons.