×

Generalized stoichiometry and biogeochemistry for astrobiological applications. (English) Zbl 1467.92009

Summary: A central need in the field of astrobiology is generalized perspectives on life that make it possible to differentiate abiotic and biotic chemical systems. A key component of many past and future astrobiological measurements is the elemental ratio of various samples. Classic work on Earth’s oceans has shown that life displays a striking regularity in the ratio of elements as originally characterized by Redfield. The body of work since the original observations has connected this ratio with basic ecological dynamics and cell physiology, while also documenting the range of elemental ratios found in a variety of environments. Several key questions remain in considering how to best apply this knowledge to astrobiological contexts: How can the observed variation of the elemental ratios be more formally systematized using basic biological physiology and ecological or environmental dynamics? How can these elemental ratios be generalized beyond the life that we have observed on our own planet? Here, we expand recently developed generalized physiological models to create a simple framework for predicting the variation of elemental ratios found in various environments. We then discuss further generalizing the physiology for astrobiological applications. Much of our theoretical treatment is designed for in situ measurements applicable to future planetary missions. We imagine scenarios where three measurements can be made – particle/cell sizes, particle/cell stoichiometry, and fluid or environmental stoichiometry – and develop our theory in connection with these often deployed measurements.

MSC:

92B05 General biology and biomathematics
92F05 Other natural sciences (mathematical treatment)
92D40 Ecology
PDFBibTeX XMLCite
Full Text: DOI arXiv

References:

[1] Anbar AD (2008) Elements and Evolution. Science 322(5907):1481-1483
[2] Andersen KH, Berge T, Gonçalves RJ, Hartvig M, Heuschele J, Hylander S, Jacobsen NS, Lindemann C, Martens EA, Neuheimer AB et al (2016) Characteristic sizes of life in the oceans, from bacteria to whales. Ann Rev Mar Sci 8:217-241
[3] Andersson A, Rudehäll Å. (1993) Proportion of plankton biomass in particulate organic carbon in the northern Baltic Sea. Mar Ecol Prog Series 95(1/2):133-139
[4] Beardall, J.; Allen, D.; Bragg, J.; Finkel, ZV; Flynn, KJ; Quigg, A.; Rees, TAV; Richardson, A.; Raven, JA, Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton, New Phytol, 181, 2, 295-309 (2009) · doi:10.1111/j.1469-8137.2008.02660.x
[5] Bremer H, Dennis PP, Neidhardt F Eds (1996) Modulation of chemical composition and other parameters of the cell by growth rate. In: Escherichia coli and Salmonella typhimurium. Cellular and molecular biology: Chapter 96. Second Edition. American society for microbiology
[6] Brown, J.; Gillooly, J.; Allen, A.; Savage, V.; West, G., Toward a metabolic theory of ecology, Ecology, 85, 7, 1771-1789 (2004) · doi:10.1890/03-9000
[7] Burmaster, DE, The continuous culture of phytoplankton: mathematical equivalence among three steady-state models, Am Nat, 113, 1, 123-134 (1979) · doi:10.1086/283368
[8] Cavender-Bares, KK; Rinaldo, A.; Chisholm, SW, Microbial size spectra from natural and nutrient enriched ecosystems, Limnol Oceanogr, 46, 4, 778-789 (2001) · doi:10.4319/lo.2001.46.4.0778
[9] Chopra A, Lineweaver CH (2008) The major elemental abundance differences between life, the oceans and the sun. In: Proceedings of the 8th Australian space science conference, Canberra, pp. 49-55
[10] Cuesta JA, Delius GW, Law R (2018) Sheldon spectrum and the plankton paradox: two sides of the same coin: a trait-based plankton size-spectrum model. J Math Biol 76(1):67-96 · Zbl 1392.92072
[11] DeLong J, Okie J, Moses M, Sibly R, Brown J (2010) Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life. Proceed Nat Acad Sci 107(29):12941-12945
[12] Edwards, KF; Thomas, MK; Klausmeier, CA; Litchman, E., Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton, Limnol Oceanogr, 57, 2, 554-566 (2012) · doi:10.4319/lo.2012.57.2.0554
[13] Nature Geoscience Editorial (2014) Eighty years of Redfield.Nat. Geosci 7: 849
[14] Elrifi IR, Turpin DH (1985) Steady-state luxury consumption and the concept of optimum nutrient ratios: a study with phosphate and nitrate limited Selenastrum minutum (chlorophyta). J Phycol 21(4):592-602
[15] Elser JJ (2003) Biological stoichiometry: a theoretical framework connecting ecosystem ecology, evolution, and biochemistry for application in astrobiology. Int J Astrobiol 2(3):185-193
[16] Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N: P stoichiometry: toward a unified view of cellular and ecosystem processes. BioScience 46(9):674-684
[17] Elser, J.; Sterner, RW; Gorokhova, E.; Fagan, W.; Markow, T.; Cotner, JB; Harrison, J.; Hobbie, SE; Odell, G.; Weider, L., Biological stoichiometry from genes to ecosystems, Ecol Lett, 3, 6, 540-550 (2000) · doi:10.1046/j.1461-0248.2000.00185.x
[18] Elser, JJ; Fagan, WF; Kerkhoff, AJ; Swenson, NG; Enquist, BJ, Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change, New Phytol, 186, 3, 593-608 (2010) · doi:10.1111/j.1469-8137.2010.03214.x
[19] Finkel, ZV, Light absorption and size scaling of light-limited metabolism in marine diatoms, Limnol Oceanogr, 46, 1, 86-94 (2001) · doi:10.4319/lo.2001.46.1.0086
[20] Finkel, ZV; Irwin, AJ; Schofield, O., Resource limitation alters the 3/4 size scaling of metabolic rates in phytoplankton, Marine Ecol Progress Series, 273, 269-279 (2004) · doi:10.3354/meps273269
[21] Finkel, ZV; Follows, MJ; Liefer, JD; Brown, CM; Benner, I.; Irwin, AJ, Phylogenetic diversity in the macromolecular composition of microalgae, PLoS One, 11, 5, e0155977 (2016) · doi:10.1371/journal.pone.0155977
[22] Finkel, Z.; Follows, M.; Irwin, A., Size-scaling of macromolecules and chemical energy content in the eukaryotic microalgae, J Plankton Res, 38, 5, 1151-1162 (2016) · doi:10.1093/plankt/fbw057
[23] Galbraith, ED; Martiny, AC, A simple nutrient-dependence mechanism for predicting the stoichiometry of marine ecosystems, Proceed Nat Acad Sci, 112, 27, 8199-8204 (2015) · doi:10.1073/pnas.1423917112
[24] Geider, RJ; La Roche, J., Redfield revisited: variability of C:N: P in marine microalgae and its biochemical basis, Eur J Phycol, 37, 1, 1-17 (2002) · doi:10.1017/S0967026201003456
[25] Hamilton, RD; Holm-Hansen, O., Adenosine triphosphate content of marine bacteria, Limnol Oceanogr, 12, 2, 319-324 (1967) · doi:10.4319/lo.1967.12.2.0319
[26] Healey FP (1985) Interacting effects of light and nutrient limitation on the growth rate of Synechococcus linearis (cyanophyceae). J Phycol 21(1):134-146
[27] Hutchinson GE (1957) Concluding remarks: Cold Spring Harbor Symposium. Quant Biol 22:415-427
[28] Hutchinson, GE, The concept of pattern in ecology, Proceed Acad Nat Sci Philadelphia, 105, 1-12 (1953)
[29] Irwin, AJ; Finkel, ZV; Schofield, OM; Falkowski, PG, Scaling-up from nutrient physiology to the size-structure of phytoplankton communities, J Plankton Res, 28, 5, 459-471 (2006) · doi:10.1093/plankt/fbi148
[30] Karr, JR; Sanghvi, JC; Macklin, DN; Gutschow, MV; Jacobs, JM; Bolival, B. Jr; Assad-Garcia, N.; Glass, JI; Covert, MW, A whole-cell computational model predicts phenotype from genotype, Cell, 150, 2, 389-401 (2012) · doi:10.1016/j.cell.2012.05.044
[31] Kempes, CP; Dutkiewicz, S.; Follows, MJ, Growth, metabolic partitioning, and the size of microorganisms, Proceed Nat Acad Sci, 109, 2, 495-500 (2012) · doi:10.1073/pnas.1115585109
[32] Kempes CP, Wang L, Amend JP, Doyle J, Hoehler T (2016) Evolutionary tradeoffs in cellular composition across diverse bacteria. ISME J 10(9):2145-2157
[33] Kempes, CP; van Bodegom, PM; Wolpert, D.; Libby, E.; Amend, J.; Hoehler, T., Drivers of bacterial maintenance and minimal energy requirements, Front Microbiol, 8, 31 (2017) · doi:10.3389/fmicb.2017.00031
[34] Kempes, CP; West, GB; Koehl, M., The scales that limit: the physical boundaries of evolution, Front Ecol Evol, 7, 242 (2019) · doi:10.3389/fevo.2019.00242
[35] Kerkhoff, AJ; Enquist, BJ; Elser, JJ; Fagan, WF, Plant allometry, stoichiometry and the temperature-dependence of primary productivity, Global Ecol Biogeogr, 14, 6, 585-598 (2005) · doi:10.1111/j.1466-822X.2005.00187.x
[36] Kim H, Smith HB, Mathis C, Raymond J, Walker SI (2019) Universal scaling across biochemical networks on Earth. Sci Adv 5(1):eaau0149
[37] Klausmeier, CA; Litchman, E.; Levin, SA, Phytoplankton growth and stoichiometry under multiple nutrient limitation, Limnol Oceanogr, 49, 4, 1463-1470 (2004) · doi:10.4319/lo.2004.49.4_part_2.1463
[38] Klausmeier, CA; Litchman, E.; Daufresne, T.; Levin, SA, Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton, Nature, 429, 6988, 171-174 (2004) · doi:10.1038/nature02454
[39] Klausmeier, C.; Litchman, E.; Levin, SA, A model of flexible uptake of two essential resources, J Theor Biol, 246, 2, 278-289 (2007) · Zbl 1451.92202 · doi:10.1016/j.jtbi.2006.12.032
[40] Klausmeier, CA; Litchman, E.; Daufresne, T.; Levin, SA, Phytoplankton stoichiometry, Ecol Res, 23, 3, 479-485 (2008) · doi:10.1007/s11284-008-0470-8
[41] Klausmeier CA, Tilman, D (2002) Spatial models of competition. In: Competition and coexistence, Eds. Sommer, Ulrich, Worm, Boris. Chap. 3, pp. 43-78. Springer, Berlin, Heidelberg
[42] Kremer, CT; Klausmeier, CA, Coexistence in a variable environment: eco-evolutionary perspectives, J Theor Biol, 339, 14-25 (2013) · Zbl 1411.92212 · doi:10.1016/j.jtbi.2013.05.005
[43] Legović T, Cruzado A (1997) A model of phytoplankton growth on multiple nutrients based on the Michaelis-Menten-Monod uptake, Droop’s growth and Liebig’s law. Ecol Model 99(1):19-31
[44] Levin, SA, Community equilibria and stability, and an extension of the competitive exclusion principle, Am Nat, 104, 939, 413-423 (1970) · doi:10.1086/282676
[45] Levins, R.; Culver, D., Regional coexistence of species and competition between rare species, Proceed Nat Acad Sci, 68, 6, 1246-1248 (1971) · Zbl 0217.57702 · doi:10.1073/pnas.68.6.1246
[46] Liefer, JD; Garg, A.; Fyfe, MH; Irwin, AJ; Benner, I.; Brown, CM; Follows, MJ; Omta, AW; Finkel, ZV, The macromolecular basis of phytoplankton C:N: P under nitrogen starvation, Front Microbiol, 10, 763 (2019) · doi:10.3389/fmicb.2019.00763
[47] Lineweaver CH, Chopra A (2012) What Can Life on Earth Tell Us About Life in the Universe?. In: Seckbach J (ed) Genesis-In The Beginning. Precursors of Life, Chemical Models and Early Biological Evolution, pp: 799-815. Springer, Dordrecht
[48] Litchman, E.; Klausmeier, CA; Schofield, OM; Falkowski, PG, The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level, Ecol Lett, 10, 12, 1170-1181 (2007) · doi:10.1111/j.1461-0248.2007.01117.x
[49] Loladze I, Elser JJ (2011) The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. Ecol Lett 14(3):244-250
[50] L \(\phi\) vdal T, Skjoldal E, Heldal M, Norland S, Thingstad T (2008) Changes in morphology and elemental composition of Vibrio splendidus along a gradient from carbon-limited o phosphate-limited growth. Microb Ecol 55(1):152-161
[51] McKay CP (2008) An approach to searching for life on Mars, Europa, and Enceladus. In: Botta O, Bada J, Gómez Elvira J, Javaux E, Selsis F, Summons R (eds) Strategies of Life Detection, pp. 49-54. Springer Science & Business
[52] Meroueh, SO; Bencze, KZ; Hesek, D.; Lee, M.; Fisher, JF; Stemmler, TL; Mobashery, S., Three-dimensional structure of the bacterial cell wall peptidoglycan, Proceed Nat Acad Sci, 103, 12, 4404-4409 (2006) · doi:10.1073/pnas.0510182103
[53] Neveu, M.; Poret-Peterson, A.; Anbar, A.; Elser, J., Ordinary stoichiometry of extraordinary microorganisms, Geobiology, 14, 1, 33-53 (2016) · doi:10.1111/gbi.12153
[54] Nichols, JW; Deamer, DW, Net proton-hydroxyl permeability of large unilamellar liposomes measured by an acid-base titration technique, Proceed Nat Acad Sci, 77, 4, 2038-2042 (1980) · doi:10.1073/pnas.77.4.2038
[55] Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46(3):205-221
[56] Rhee G-Y (1973) A continuous culture study of phosphate uptake, growth rate and polyphosphate in Scenedesmus sp. J Phycol 9(4):495-506
[57] Rhee G-Y (1978) Effects of N: P atomic ratios and nitrate limitation on algal growth, cell composition, and nitrate uptake. Limnol Oceanograp 23(1):10-25
[58] Savage, V.; Gillooly, J.; Woodruff, W.; West, G.; Allen, A.; Enquist, B.; Brown, J., The predominance of quarter-power scaling in biology, Func Ecol, 18, 257-282 (2004) · doi:10.1111/j.0269-8463.2004.00856.x
[59] Savage, V.; Gillooly, J.; Brown, J.; West, G.; Charnov, E., Effects of body size and temperature on population growth, Am Nat, 163, 3, 429-441 (2004) · doi:10.1086/381872
[60] Sheldon, R.; Parsons, T., A continuous size spectrum for particulate matter in the sea, J Fisheries Board Canada, 24, 5, 909-915 (1967) · doi:10.1139/f67-081
[61] Shuler, M.; Leung, S.; Dick, C., A mathematical model for the growth of a single bacterial cell, Ann New York Acad Sci, 326, 1, 35-52 (1979) · doi:10.1111/j.1749-6632.1979.tb14150.x
[62] Sterner, RW; Andersen, T.; Elser, JJ; Hessen, DO; Hood, JM; McCauley, E.; Urabe, J., Scale-dependent carbon: nitrogen:phosphorus seston stoichiometry in marine and freshwaters, Limnol Oceanogr, 53, 3, 1169-1180 (2008) · doi:10.4319/lo.2008.53.3.1169
[63] Szalontai B, Nishiyama Y, Gombos Z, Murata N (2000) Membrane dynamics as seen by Fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803: the effects of lipid unsaturation and the protein-to-lipid ratio. Biochim Biophys Acta Biomembr BBA-Biomembranes 1509(1-2):409-419
[64] Tang, EP, The allometry of algal growth rates, J Plankton Res, 17, 6, 1325-1335 (1995) · doi:10.1093/plankt/17.6.1325
[65] Taniguchi, DA; Franks, PJ; Poulin, FJ, Planktonic biomass size spectra: an emergent property of size-dependent physiological rates, food web dynamics, and nutrient regimes, Mar Ecol Progr Series, 514, 13-33 (2014) · doi:10.3354/meps10968
[66] Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, USA
[67] Verdy, A.; Follows, M.; Flierl, G., Optimal phytoplankton cell size in an allometric model, Mar Ecol Progr Series, 379, 1-12 (2009) · doi:10.3354/meps07909
[68] Volterra V (1926) Variazioni e fluttuazioni del numero d’individui in specie animali conviventi. Memoria della Reale Accademia Nazionale dei Lincei 2: 31-113 · JFM 52.0450.06
[69] Volterra V (1931) Leçons sur la Théorie Mathématique de la Lutte pour la Vie, Gauthier-Villars, Paris · JFM 57.0466.02
[70] Vrede, T.; Dobberfuhl, DR; Kooijman, S.; Elser, JJ, Fundamental connections among organism C:N: P stoichiometry, macromolecular composition, and growth, Ecology, 85, 5, 1217-1229 (2004) · doi:10.1890/02-0249
[71] Wang HS, Lineweaver CH, Ireland TR (2018) The elemental abundances (with uncertainties) of the most Earth-like planet. Icarus 299:460-474
[72] Ward, BA; Dutkiewicz, S.; Jahn, O.; Follows, MJ, A size-structured food-web model for the global ocean, Limnol Oceanograp, 57, 6, 1877-1891 (2012) · doi:10.4319/lo.2012.57.6.1877
[73] West, G.; Brown, J., The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization, J Exp Biol, 208, 9, 1575-1592 (2005) · doi:10.1242/jeb.01589
[74] Young, PA; Desch, SJ; Anbar, AD; Barnes, R.; Hinkel, NR; Kopparapu, R.; Madhusudhan, N.; Monga, N.; Pagano, MD; Riner, MA, Astrobiological stoichiometry, Astrobiology, 14, 7, 603-626 (2014) · doi:10.1089/ast.2014.1143
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.