A_C_T_A_-_v_o_L_._1_4_-_N_0 6---~~--- ______________________________________ o_c_E_A_N_O_L_O_G_IC_A __ The biological use of chemical elements: selection on environmental availability and electron configuration Elemental composition Biological material Environmental availability Oceanic residence time Composition élémentaire Matière biologique Disponibilité Temps de résidence Dirk H. SPAARGAREN Netherlands Institute for Sea Research, P.O. Box n° 59, 1790 AB Den Burg, Texel, The Netherlands. Received 25/04/91, in revised form 23/08/91, accepted 2/09/91. ABSTRACT The molal concentrations of 34 elements in marine organisms were compared with the availability of these elements in their natural environment and sorne physicochemical properties of the elements,viz. the charge/radius ratio or ionie potential and the "noble gas deviation" or NGD-index. The NGD-index is defined in this paper as a value which expresses the deviation of the electron configuration of an element with that of the previous and subsequent noble gas configurations. The value for the NGD-index can be obtained by multiplying the number of electrons which must be lost or gained to obtain the configuration of, respectively, the previous and the subsequent noble gas, divided by their squared sum. The concentration factor (ratio of element concentration in biological material and in the environment) appears to be a periodic function of the element number, very similar to the NGD-index. The relation is most obvious when the composition of biological material is compared with that of sea water and river water and becomes Jess clear in the comparison with the composition of crustal rocks. These results do not exclude a freshwater origin of marine organisms. The close fit between the concentration factor and the NGD-index offers, with sorne limitations, a possibility to assess the concentration factors of elements for which up till now no data have been available. · Oceanologica Acta, 1991. 14, 6, 569-574. RÉSUMÉ Utilisation biologique d'éléments chimiques: sélection en fonction de la disponibilité dans le milieu et de la configuration électronique · Les compositions molaires de 34 éléments présents dans les organismes marins ont été comparées à leur abondance dans le milieu naturel et à quelques propriétés physico-chimiques de ces éléments, à savoir le rapport charge/rayon ou le potentiel ionique et «l'écart par rapport au gaz noble» ou indice-NGD. L'indice NGD est défini dans cet article comme l'écart entre la configuration électronique d'un élément et celle des gaz nobles qui le précèdent ou le suivent. La valeur de l'indice-NGD s'obtient en multipliant les nombres d'électrons à perdre ou à gagner pour obtenir la configuration du gaz noble qui précède ou qui suit, et en divisant le résultat par le carré de leur somme. Le facteur de concentration (rapport de la concentration de l'élément dans la matière biologique et dans le milieu) semble être une fonction périodique du numéro de l'élément, très similaire à l'indice-NGD. La relation est la plus nette lorsque la 0399-1784/91/06 569 06/$ 2.60/© Gauthier-Villars 569 D.H. SPAARGAREN matière biologique est comparée à l'eau de mer et à l'eau fluviale ; elle est moins claire dans la comparaison avec la composition des roches de la croûte. Ces résultats n'excluent pas que les organismes marins proviennent de l'eau douce. L'ajustement serré entre le facteur de concentration et l'indice-NGD permet, dans certaines limites, d'évaluer les facteurs de concentration des éléments pour lesquels aucune donnée n'était disponible jusqu'à présent. Oceanologica Acta, 1991. 14, 6, 569-574. INTRODUCTION DATA AND DATA PROCESSING For about 40 chemical elements reasonably accurate values are available regarding their presence in living organisms (e.g. Vinogradov, 1953; Sidwell et al., 1977; 1978; Yamamoto et al., 1980; Eisler, 1981). From these datait appears that the basic elemental composition of living organisms is fairly stable. No significant difference could be shown to exist between marine, freshwater or terrestrial organisms (Bannin and Navrot, 1975). In ail organisms sampled the elements H, 0, C and N are present in molar concentrations and the elements Na, Mg, Si, P, Cl, K and Ca occur in millimolar concentrations. Most metals occur in micromolar concentrations while a large number of remaining elements are present in nanomolar concentrations. Although in different species the element concentrations are widely variable, and can show a variation of up to two orders of magnitude, it may be postulated that the ratios in which various elements co-occur remain approximately constant (Banin and Navrot, 1975; Gualtieri, 1977; Spaargaren, 1985 a). The similarity in elemental composition in species from widely diverging taxonomie groups is probably related to the fact that many biochemical processes are similar for ali organisms [and were possibly established already during the early stages in the development oflife (e.g., Oparin, 1972)]. Data on the elemental composition (in the soft parts) of a large number of marine teleosts, molluscs and crustaceans were obtained from a previous study (Spaargaren, 1985 a) in which concentration values (in moles/kg fresh weight; Tab. 1) of various elements, compiled by Sidwell et al. (1977; 1978), were analysed statistically. Data on the chemical composition of sea water were drawn from tables in Brewer (1975, 417-421) and Bruland (1983, 172-173). Those on the average elemental composition of river water and crustal rocks were obtained from a table in Turner et al (1980). The elemental composition of biological material was compared with that of their natural environments as weil as related to two physicochemical properties of the elements, viz. their NGD-index (see below) and their ionie potential. The "noble gas deviation" or NGD-index, is a value describing the capacity of an element to share electrons in the outer electron orbitais with other atoms. To obtain a stable noble gas configuration an element must loose or gain a number of electrons in the outer s, p and d orbitais. The number of electrons which must be Iost to reach the configuration of the previous noble gas multiplied by the number of electrons which must be gained to obtain the configuration of the next subsequent noble gas gives a index for the combined chances. The quantity can be made dimensionless by dividing the obtained value by the squared sum (viz. the total number of electrons involved) of the above numbers. Its value can most easily be derived from the equation: The large number of elements that are only present in very low concentrations contain various substances for which it is unclear whether they are actually involved in vital processes. Egami (1974) made a distinction between useful, neutral and toxic elements. He assumed that only those elements which in the primordial environment were present in sufficiently high concentrations became involved in biological processes. Below a criticallevel of 1 to 5 nmol/kg they were excluded from organic evolution. In the latter case organisms developed independently, gaining neither the capacity to use these elements nor the capacity to tolerate them. The distinction as proposed by Egami is not always very clear. Essential elements may appear to be toxic in high concentrations. Several elements which were supposed to be toxic were at a later stage found to be essential (in low concentrations). Environmental availability is important for the biological use of chemical elements but, undoubtedly, the chemical properties of the elements must also have been critical for their incorporation in biologica1 material (Williams, 1981 ). This paper seeks to provide further insight as to why various chemical elements occur, and most probably are utilized, in such strongly varying quantities. NDG =(Z - Zp).(Zs - Z)/(Zs - Zp) 2 in which Z represents the atomic number of the element and Zp and Z 8 represent the atomic number of respectively the previous and next subsequent noble gas. From this definition it is clear that the NGD-index can not be determined for hydrogen and the actinids. The numerical values for the NGD-index thus defined range from zero (for the noble gases) to 0.25 (for elements in the centre of each period of the periodic system). The ionie potential of an element is defined (e.g. Banin and Navrot, 1975; Dileep Kumar, 1983; 1984) as the ratio between the charge and the radius of an ion. Ionie radii of the elements are given in the handbook of Chemistry and Physics (e.g. Weast, 1970). Values for the ionie potential were calculated using the valency of the naturally most abundant state of an ion (e.g. Brewer, 1975). 570 BIOLOGICAL USE OF CHEMICAL ELEMENTS Log(Cbiol) RESULTS 2 Relations between biological and environmental concentrations 0 -2 Generally speaking, the concentrations of chemical elements in living material decrease with increasing atomic weight (Fig. 1). This relation may be somewhat misleading because of the fact that for many elements, especially those occurring in very low concentrations, no data are available. Within each period of the periodic system large changes in the biological concentrations occur. Boron (and probably also lithium and the very rare beryllium) from the second period, together with fluorine, have exceptionally low values compared to C, N and 0 from the same period. In the third period, aluminium shows an aberrant, very low, position. In the fourth period, a sharp decrease is found for elements having an element number higher than 20 (Ca); higher concentrations are gradually restored when reaching -4 -s -a -10 -12 -l 4 -!:o--l:r:-0---,2r-O--3:r0:---4r0---,5r-O--s'o--7ro---,er-o....:.:::.::..jso ATOMIC NUMBER Figure 1 Average elemental composition of biological material. Plotted are the logarithms of the molal concentrations in living material (whole animais, skeleton removed prior to analysis) as a function of the atomic numbers of the elements. Table 1 Average biological, sea water, river water and crustal rock concentration (in moles/kg) in relation to atomic number and NGD-index. Element/nr NGD Ag Al As B Be Br 47 13 33 5 4 35 c 6 Ca 20 Cd 48 Cl 17 Co 27 Cr 24 Çu 29 F 9 Fe 26 H 1 Hg 80 1 53 K 19 Li 3 Mg 12 Mn 25 Mo42 N 7 Na 11 Ni 28 0 8 p 15 Pb 82 Ra 88 Rb 37 s 16 Sb 51 Sc 21 Se 34 Si 14 Sn 50 Sr 38 Ti 22 v 23 Zn 30 F 0.238 0.234 0.139 0.234 0.188 0.053 0.25 0.099 0.222 0.109 0.25 0.222 0.238 0.109 0.247 0.222 0.053 0.053 0.109 0.188 0.238 0.222 0.234 0.109 0.247 0.188 0.234 0.173 0.053 0.188 0.139 0.139 0.099 0.25 0.173 0.099 0.173 0.201 0.222 cbiol 8.95E-4 5.67E-5 2.04E-3 1.50E-3 7.89 1.54E-2 2.41E-6 4.95E-2 9.19E-6 3.34E-6 7.84E-5 1.03E-4 3.92E-4 7.38E+l 2.51E-6 l.OOE-5 7.90E-2 1.38E-2 2.56E-5 5.79E-6 1.63E+O 4.19E-2 2.95E-6 4.23E+1 7.48E-2 9.48E-6 2.63E-14 4.26E-2 6.75E-6 4.47E-2. l.SIE-5 2.88E-3 3.16E-5 9.01E-6 3.56E-4 Csea 3.71E-10 1.85E-8 2.00E-8 4.11E-4 6.31E-10 8.39E-4 2.29E-3 1.03E-2 8.90E-ll 5.50E-1 8.48E-10 5.77E-9 1.57E-9 6.76E-5 3.58E-8 1.10E+2 1.51E-10 5.01E-7 9.72E-3 2.59E-5 5.31E-2 3.64E-9 1.04E-7 1.07E-2 4.68E-1 3.41E-9 5.50E+1 1.94E-6 1.45E-11 3.02E-16 1.40E-6 2.82E-2 1.97E-9 1.33E-11 2.51E-9 7.12E-5 8.32E-11 9.13E-5 2.09E-8 4.91E-8 1.53E-9 Criver Crock 2.78E-9 1.85E-6 2.27E-8 1.66E-6 6.49E-10 2.57E-3 1.05E-7 6.01E-6 3.09E-4 5.01E-8 1.66E-2 1.12E-3 1.78E-9 3.63E-3 2.21E-7 1.37E-6 5.04E-7 3.31E-2 6.43E-4 2.50E-7 1.05E-4 3.32E-4 1.78E-10 5.01E-5 3.39E-9 1.92E-8 2.36E-8 5.25E-6 7.16E-7 1.11E+2 3.47E-10 5.50E-8 3.84E-5 1.73E-6 1.28E-4 1.49E-7 5.21E-9 1.86E-5 2.31E-4 8.52E-9 l.OOE+2 3.71E-6 4.83E-10 1.76E-8 1.20E-4 8.21E-9 8.90E-11 2.51E-9 1.78E-4 3.39E-10 6.85E-7 2.09E-7 1.96E-8 4.59E-7 the last element (Br) of this period. In the fifth period a decrease sets in at element number 42 (molybdenum). A similar negative relation between element concentration and atomic number is also found in the elemental composition of natural environments such as sea water and river water (e.g. Tab. 1). Such a similarity already implies that the chemical composition of biological material is, in great measure, related to the environmental availability of the various elements. Despite the similarities, very large differences between the biological concentrations and environmental concentrations can occur. These differences, usually expressed as concentration factors (the ratio between biological and environmental concentration), can be as large as a factor 106 (Fig. 2). Especially the concentrations of the heavier metals in biological material are often much higher than their environmental values. Non-metal atoms (e.g. halogens) are usually concentrated to a lesser extent; the concentration factors for Cl, Br and I appear to be positively related to their atomic weight. 3.98E-7 3.98E-6 6.24E-4 6.05E-6 6.75E-4 1.31E-5 1.77E-8 1.41E-3 6.18E-4 8.35E-7 Although part of the biological composition can be explained from the point of environmental availability, the occurrence of very variable concentration factors makes it clear that other factors are involved in the biological utilization of chemical elements. It is very likely that the remaining differences must be ascribed to specifie chemical properties of the elements. 1.97E-5 7.72E-8 1.31E-6 7.94E-3 7.39E-9 2.29E-7 6.31E-7 9.79E-3 1.70E-5 3.17E-6 7.93E-5 1.90E-6 1.94E-6 Relation between concentration factors and electron configuration of the elements When concentration factors (biological concentrations with respect to seawater concentrations) are plotted against atomic numbers (Fig. 2), a characteristic pattern appears with high concentration factors for elements near the middle of each period, decreasing to low values for elements positioned more closely to the noble gases. This pattern suggests 571 D.H. SPAARGAREN 10 6 Figure 2 Concentration factors (CbiotiCsea water: symbols referring to the left-hand ordinate) and NGD-index (dotted line, right-hand ordinale) as a function of atomic number 0.3 Sn • 10 5 ...... - Pb Hg Cl.) .. • 10 4 CQ 0.25 ··~:d 3: CQ Cl.) • ·.• z 1000 (;') Ill ü ....... . 100 RI • lllo Sr ;• : 10 0 0.20 1 ::Il 1 Q.. • CD >< 0 .0 0.15 ü Cl • 0.1 0.01 -+------,----;----r-----.----r 0 18 36 54 72 0.1 90 A ternie number that the concentration factors are related to the electron configuration of the elements. Noble)'.Îses have complete! y filled outer electron orbitais. The adjacent alkali metals and halogens only have to loose or to gain one electron to obtain a noble gas configuration, whereas the other elements show larger deviations from the stable noble gas configuration. A simple way to characterize the deviation from the previous and subsequent noble gas configurations is given by the NGD-index as defined above. The dotted lines in Figure 2 illustrate this index and it is clear that the NGD-index is closely related to the concentration factors of the various elements. It is not possible directly to relate the NGD-index in a simple way to the chemical reactivity of an element. In an attempt to explain the observed relation one might consider that a high NGD-index indicates that an element has many possibilities to improve its stability. The tendency to reach a (near) noble gas configuration may provide a reason as to why the elements with a high NGD-index become easily incorporated in complex molecules constituting living matter. This may indicate that other, yet unknown, factors are also involved. The exceptions may also partly be ascribed to inaccuracies in the available data. The concentration factors are based on values for the average element concentration, both in biological material and in seawater. Both values may suffer from a certain inaccuracy and especially the biological concentrations often show a large interspecific variation of one or two orders of magnitude. For silicon, for instance, the analytical method for its determination requires the silicon present to be processed to a soluble form. This is a very tirne-consuming process and it may be that incomplete sample treatment is the reason for the low silicon concentrations reported for living material. With the exception of hydrogen (for which the NGD-index can not be derived properly), silicon and nickel, ali other deviating concentration factors suggest a biological concentration which is too high with respect to the sea water concentration of the element. Most obvious is the value for tin, but also the values for mercury, lead, strontium and radium are too high to be explained by the NGD-index. This again may reflect the inaccuracy of the data. Tin determinations in biological material, for instance, stem mainly from measurements on canned food. Renee, its not so surprising that, due to contamination, a relatively high concentration factor for this element is reported. Also the values for mercury, lead,strontium and radium may be biased by the selection of the samples. The positive deviations for Sn, Hg and Pb may also be explained by their increased ocean input during the last decades (Li, 1981; Patterson 1987). The concentration factors of most elements closely follow the NGD-index (Fig. 2), but there are a few exceptions. Table 2 Correlations between the elemental composition of biological material, sea water, river water, crustal rock and chemical reactivity (NGD-index: see text). Concentrations in the various biogeochemical reservoirs in moles/kg. Corr. coeff. N log Cbiol = 8.3151 NGD + 0.5574log Csea- 1.5405 log Cbiol 1.4074 NGD + 0.7537log Criver+ 1.2173 log Cbiol =- 1.2049 NGD + 0.6789log Crock + 0.1023 0.8944 33 0.8941 33 0.7219 32 log Csea = - 12.3407 NGD + 1.25521og Criver + 4.2767 log Csea 15.5403 NOD+ 1.0030 log Crock + 1.5072 0.9256 38 0.7246 38 log Criver =- 2.4638 NGD + O. 7822 log Crock - 2.27 40 0.8299 37 = =- DISCUSSION In general, the data for the concentration factors of various elements fit very weil with the levels as predicted by the NGD-index mode!. Figure 2 (as weil as the first regression equation in Tab. 2) offers, with sorne limitations, a possibility to assess concentration factors for elements for which 572 BIOLOGICAL USE OF CHEMICAL ELEMENTS up till now no data have been available. The limitations concern the facts that the NOD-index cannat be derived for aU elements (not for hydrogen and actinids) and that accurate date for the sea water concentrations must be available. Figure 2 moreover shows that there are sorne exceptions that cannot yet be explained. For this reason one al ways has to be very cautious with those calculated values. From the results it seems , however, safe to postulate that, together with element availability, the configuration of the outer electron orbitais strongl y determines the likelihood that an element is incorporated in biological material. The outer electron orbitais strongly determine the chemical properties of an element, but from this knowledge it is not yet poss ible to give a complete explanation for the observed relation . For the moment it seems that elements with a high NOD-index have more chances to improve their stability by the formation of large, complex molecules than the more noble elements and therefore have more chances to become incorporated in living matter. Loo(Cbioll For limited series of close]y related elements (e.g. the rare earths), clear linear relations between the abundance of an element and its ionie potential have been fou nd (Dil eep Kumar, 1983; 1984). A plot of the element concentrations in marine organisms and sea water against their IP-values yields "V"-shaped patterns (Fig. 3). Elements with poorly so luble hydroxides are located in the middle range of IFvalues; at more extreme IP-values, the soluble oxyanions and the cations with a thick water envelope are found. The patterns are most clear for sea water (Fig. 3 b). For marine organisms (Fig. 3 a) the V-shape is also present; for fresh water and for crustal rock it is nearly absent. Banin and Navrot ( 1975) presented si m il ar plots of the element concentrations in various biological material (bacteria, fungi, plants, terrestrial animais, etc.) and sea water as a function of their ionie potential. The similarity between the patterns lead them to the conclusion that living organisms had a marine origin (opposing the panspermia hypothesis of Crick and Orgel (1973) who suggested an extraterrestrial Loo(Cseo woter) -1 Figure 3 -3 Elemental concentrations in hiological material (a) and sea water (b) in relation to the ionie potential (charge/radius ratio) of the elements. -5 -7 -9 a -11+----.---.....-----.----,---' -0.2 0.2 0.6 1.0 1.4 Log (ionie potentiol) Lo9 (ionie potential) The NOD-index as derived here is not the only criterion for explaining element abondances. Another useful criterion might be the ionie potential (IP) of elements (Ban in and Navrot, 1975; Dileep Kumar, 1983; 1984). The ionie potential, defined as the ratio between charge and radius of an ion, is a measure of the interaction of an element with water molecules. Positive ions are attracted by the oxygen atom in the polar water molecule and compete with the hydrogen ions. With low values for the ionie potential (log IP < 0.5) the interaction is weak, but the ion will attract an envelope of water molecules which will keep the ion in so lution. At intermediate IP-values (0.5 <log IP < 1.0), the attractive forces of the cation and the hydrogen ions will be of the same order of magnitude , resulting in the formation of a usually insoluble hydroxide. At still higher IP-values (log IP > 1.0) a usually soluble oxyanion is formed whereas the hydrogenion s are completely expelled from the water molecule. origin of life). The strong covariance between the element composition of aU living matter and that of sea water will, however, always evoke similar patterns (Spaargaren, 1985 b); therefore, the argument of Banin and Navrot might be not justified. Similarities in elemental composition of biogeochemical reservoirs, might, as suggested by Banin and Navrot, give sorne elues to their origin. Table 2 shows multiple linear regression fits of element concentrations in marine organism s, related to the NOD-index and the environmental concentrations. The elemental composition of biological material appears to be closely related to that of sea water and fresh (river) water; the relation with crustal rock composition is rather poor. The composition of sea water is also very weil related to that of river water; the connection with the composition of crustal rock is again fairly poor. The concentrations of various elements in sea water are positi vely related to the corresponding river or crustal rock 573 D.H. SPAARGAREN concentrations but an inverse effect of the NGD-index is observed: elements with a high NGD-index, preferentially accumulated in marine organisms, show reduced concentrations in sea water. The composition of crustal rock is most closely related to that of river water. The results as presented in Table 2 do not exclude a freshwater origin of marine organisms and may in fact support the idea of reduced ion concentrations in praebiotic oceans (Spaargaren, 1985 b). In the literature an inverse relation is reported between biologica1 concentration factors and the oceanic residence times (t) of various elements (e.g. Yamamoto, 1972; Yamamoto et al., 1980; Spaargaren and Ceccaldi, 1984). From the first equation in Table 2 it can be seen that the turnover of elements through the biogeochemical compartments can therefore also be related to their natural ahundance and the NGD-index according to: The above results demonstrate that a strong accumulation of certain elements (e.g. heavy metals) in biological material does not necessarily reflect an effect of pollution, but may merely indicate that the chemical properties of the element, as presented by its NGD-index, facilitate incorporation in biological material. 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