The biological use of chemical elements : selection on

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o_c_E_A_N_O_L_O_G_IC_A
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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.
Log t = a · Log Csea - b · NGD - c
(a, b, and c being (positive) constants). The lowest turnover rates (longest oceanic residence times, for instance
for Na and Cl), are indeed observed for those elements
which combine a the highest sea water abundance and a
low NGD-index.
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