This document discusses the history and development of using soil microbial biomass as an indicator of environmental impacts on soil ecosystems. In the 1980s, ecosystem research projects aimed to quantify the effects of pollution. Researchers realized the soil microbe compartment was important for nutrient cycling. Direct observation methods were inadequate, but the chloroform fumigation incubation technique allowed quantifying total microbial biomass. The authors then developed using maximum CO2 output of soils in relation to microbial biomass to assess environmental stress on soil microbes. This built on prior work establishing the concept of microbial maintenance energy, the energy microbes require to maintain themselves even without growth.

1. Soil Biology & Biochemistry 42 (2010) 2039e2043
Contents lists available at ScienceDirect
Soil Biology & Biochemistry
journal homepage: www.elsevier.com/locate/soilbio
Soil microbial biomass: The eco-physiological approach
Traute-Heidi Anderson a, b, c, *, Klaus H. Domsch c
a
vTI, Federal Research Institute for Rural Areas, Forestry and Fisheries, Institute of Agricultural Climate Research, Bundesallee 50, D-38116 Braunschweig, Germany
b
Federal Research Centre of Agriculture, Institute of Agroecology, Braunschweig, Germany
c
Federal Research Centre of Agriculture, Institute of Soil Biology, Braunschweig Germany
a r t i c l e i n f o a b s t r a c t
Article history: In the 1980s ecosystem research projects were implemented world-wide since there was a pressing need
Received 16 June 2010 to quantify the impacts of anthropogenic pollutants. Soil ecosystem analyses concentrated first on the
Accepted 18 June 2010 quantification of the element and energy transfer between pools. Since mineralization of organic
Available online 23 July 2010
substrates and the release of nutrients and elements are due to the heterotrophic activity of the microbial
decomposer compartment, this subsystem of terrestrial ecosystems gained importance. Direct micro-
Keywords:
scopic observation methods were inadequate for the quantification of environmental impacts on the
Soil microbial biomass
microflora. We adopted the maintenance requirement concept for the quantification of environmental
Eco-physiology
Maintenance energy demand
impacts or stress effects on the soil microbial community. The paper gives a brief inside to the concept of
Specific respiration (qCO2) maintenance from autecological studies and describes the underlying points which lead to our experi-
Stress indicator mental approach of its application at the synecological level (i.e., microbial biomass as a single ecological
Cmic-to-Corg ratio entity) e a process which rested on long-term continuous research.
Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction (1994e1998), all implemented at the Forest Ecosystem Research
Center of the University of Göttingen and funded by the former
In the 1980s ecosystem research projects were implemented Federal Ministry of Research and Technology (BMFT). The three
world-wide. Global pollution, which had led to forest decline, dying much cited SBB papers which form the basis of this article
lakes and thinning of the ozone layer was a pressing environmental (Anderson and Domsch, 1989, 1990, 1993) arose from our partici-
issue. These concerns continue to this day alongside those pation in the various follow-up projects. Of course the articles were
prompted by elevated CO2 concentrations in the atmosphere and based on a number of antecedent papers. Some of these are also
global warming. Thirty years ago there was a lack of empirical discussed below, and were products of long-term, continuous
knowledge about how soil ecosystems function (Jarvis, 1987) yet research: research which was seen as a great challenge since the
a pressing need to quantify the impacts of anthropogenic pollut- study of microbial eco-physiology in situ was in its infancy.
ants. The realisation of the scale of our ignorance led to a great Almost thirty years ago ecosystem analyses concentrated on
increase in funding and initiated a boom in ecosystem research. A input/output analysis of fluxes. It was necessary to quantify the
number of these studies were follow-ups of projects of the Inter- element (e.g., C, N, P) and energy transfer between pools and to us
national Biological Program (IBP) of the sixties and seventies, which this seemed to be the most promising approach to understanding
in many ways, represented the first steps to ecosystem analysis. the function of an ecosystem. At first, the major emphasis was
One important branch of the IBP research in Europe was the Solling element dynamics and since mineralization of organic substrates
Project in Lower Saxony (Germany). This was based at the Georg- and the release of nutrients and elements are due to the hetero-
August-University of Göttingen (Ellenberg, 1986) with follow-up trophic activity of the microbial decomposer compartment, this
projects such as “Ecosystems on Limestone Rocks” (SFB 135, subsystem of terrestrial ecosystems gained importance. For the soil
1981e1982), “Conditions of Stability of Forest Ecosystems” biologist it became obvious that direct microscopic observation
(1989e1993) and “Dynamics of Change of Forest Ecosystems” methods, even after staining and plating techniques, were inade-
quate for the quantification of the total soil microflora as the factors
used to convert microbial biovolume to microbial biomass or
biomass-C rested on unproven assumptions (Jenkinson and Ladd,
* Corresponding author at: vTI, Federal Research Institute for Rural Areas,
1981). It was, therefore, a fortunate circumstance that the Roth-
Forestry and Fisheries, Institute of Agricultural Climate Research, Bundesallee 50,
D-38116 Braunschweig, Germany. Tel.: þ49 531 596 2541; fax: þ49 531 596 2699. amsted chloroform-fumigation incubation technique (CFIM) for the
E-mail address: heidi.anderson@vti.bund.de (T.-H. Anderson). quantification of the total microbial biomass (bacteria plus fungi)
0038-0717/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.soilbio.2010.06.026

2. 2040 T.-H. Anderson, K.H. Domsch / Soil Biology & Biochemistry 42 (2010) 2039e2043
was published at this time (Jenkinson and Powlson, 1976). The early experimentally that not all the carbon supplied was used for
comprehensive ecosystem models which were generated, i.e., the growth because a portion of it was used for maintaining the cell
carbon and nitrogen cycle (e.g., Jenkinson and Rayner, 1977; Van integrity and viability of the existing population. He called this
Veen and Paul, 1981; Parton et al., 1987), took advantage of this “endogenous metabolism” since even at zero growth rate a carbon
technique. [N.B. A description of the land mark CFIM paper appears substrate demand remained; endogenous metabolism was
in Citation Classic I (Jenkinson et al., 2004)]. In addition, it was later termed “the specific maintenance rate” (a) (Marr et al., 1963).
ground-breaking and offered many new approaches to studies of Pirt (1965) building on the work of Marr et al. (1963) and
soil microbial ecology. Our colleague, John Anderson, who at that also Schulze and Lipe (1964) introduced the terms maintenance
time was screening a great number of soils to determine the fungal energy demand or “maintenance coefficient” (m, g substrate
to bacterial respiratory response (Anderson and Domsch, 1975) gÀ1 biomass hÀ1). The portion of a maintenance energy demand is
came across Jenkinson and Powlson’s publication whilst doing expressed as substrate (s) consumed per unit cell mass per unit
a literature search. The excitement was great and discussions time: thus, (ds/dt)M ¼ Àmx. Pirt (1982) refined this maintenance
followed if the CFIM method could be used in combination with the concept of microorganisms further by introducing a constant
maximal CO2 output of soils to achieve a regression between maintenance energy requirement independent of growth, the
microbial biomass (based on CFIM) and the maximal CO2 output of energy needed for maintaining cell integrity (synonymous with the
soils. Subsequently, John and Klaus Domsch (Anderson and endogenous metabolism of Herbert, 1958) and a growth rate
Domsch, 1978) developed a physiological method for the quantifi- dependent maintenance requirement which could be the produc-
cation of microbial biomass which is known today as the substrate- tion of energy storage products. Since the concept of maintenance
induced respiration technique (SIR), a method which relies on demand was to be transferred to soil organisms growing under
calibration with the fumigation technique. It is the method which extremely carbon-limited conditions (Lynch, 1979) and with
we used further on in our laboratory. very long generation times (Nedwell and Gray, 1987) it became
The relationship between dead primary products (litter), soil obvious that endogenous respiration would be the most important
organic matter (Corg) and soil microbial biomass (Cmic) became an portion of the total maintenance requirement. Hence, for practical
important issue in soil microbial ecology with respect to soil purposes the term m in our studies included the amount of external
ecosystem analyses in the eighties. The key question was how do carbon needed for energy purposes and which are either cata-
these carbon sources affect microbial productivity? Physiological bolised immediately and/or are laid down as reserve material
terms used in ‘autecological’ studies (i.e., eco-physiological studies for energy utilization at a later stage. The maintenance energy
at the species level) such as the maintenance carbon requirements, debate continues and a recent publication by Van Bodegom (2007)
growth rate, yield or turnover time were adopted and discussed appeared where the former concept of maintenance is questioned,
with respect to the soil microbial community (e.g., Babiuk and Paul, particular with respect to the definition of maintenance and
1970; Gray and Williams, 1971; Parkinson et al., 1978; McGill et al., generated equations. It is beyond the scope of this paper to take up
1981). In particular we were attracted to the concept of ‘mainte- this debate since its application to soil microbial biomass will
nance’ which was originally tested with axenic cultures (McGrew necessitate some thought and interpretation. Former extrapolated
and Mallettte, 1962; Marr et al., 1963; Pirt, 1965). The adoption of specific maintenance rates for soil microbes were in the range
the maintenance requirement concept and the study of its appli- 0.003e0.04 g substrate gÀ1 biomass hÀ1 (Babiuk and Paul, 1970;
cation at the synecological level (i.e., microbial biomass as a single Shields et al., 1973; Behera and Wagner, 1974; Barber and Lynch,
ecological entity) was the basis for our three SBB papers. 1977; Paul and Voroney, 1980). However, these values frequently
exceeded the carbon input data to a soil calculated on a yearly basis
2. Maintenance energy demand and soil microbial biomass and it became clear that the total maintenance demand of growing
cells without carbon limitations must be different from organisms
The close relationship between ecology and microbial physi- in a carbon-limited natural environment.
ology is encapsulated in the term eco-physiology. In the early days For the quantification of carbon cycle interrelationships via
(during the 1950s and 1960s) the study of ecological parameters microbial biomass and determinations of microbial turnover times
(e.g., temperature, pH, oxygen supply, nutrients) and their influence in terrestrial systems, the maintenance carbon requirement of
on microbial physiology were conducted under in vitro conditions the total microbial biomass would have to be subtracted from an
using either batch culture or continuous culture techniques and estimated total carbon pool. Since maintenance coefficients had not
concentrating at the response of one species at a time. To simulate been established under in situ conditions we accepted the chal-
more natural milieus and substrate competition between microor- lenge and this was for us the first step towards an experimental soil
ganisms, the pure culture experiments were followed by mixed microbial ecology.
culture studies. The real pioneers here were Hans Veldkamp and
Holger Jannasch (Veldkamp and Jannasch, 1972; Jannasch and 3. Testing the applicability of eco-physiological parameters
Mateles, 1974; Veldkamp, 1976). Although it is nowadays taken for at the synecological level
granted that properties of microorganisms measured under in vitro
conditions do have relevance to events in the natural environment, As mentioned above knowledge about the physiological
when we embarked upon our ecological studies, it was a highly responses of organisms to environmental factors has been gained
controversial issue in the literature. The informative reviews by from autecological studies. We followed the assumptions made by
Gray and Williams (1971), Tempest (1978), Tempest and Neijssel Tempest et al. (1984), that principles and mechanisms of growth or
(1978), Lynch and Poole (1979) and Tempest et al. (1983) were survival under axenic conditions have relevance to cells of a total
key publications back then and helped us to become acquainted multi-species community when considered as a single ecological
with this subject matter. entity. However, the specific rate constants of cell activities (e.g.
When the chemostat culture technique was applied to under- growth or maintenance) may not be transferable. When we began
stand the relationship between growth and utilization of a carbon our studies on physiological parameters, the term “activity” was
source in bacteria, the term “yield”, Y, was introduced (Herbert, widely used in soil microbiology. For instance, the respiratory
1958): Y is ¼ Àdx/ds where dx is the increase in biomass and ds is “activity” was at that time related to a weight or volume of soil and
the amount of carbon substrate used. Herbert (1958) showed not to the actual quantity of microbial cells under study. In strict

3. T.-H. Anderson, K.H. Domsch / Soil Biology & Biochemistry 42 (2010) 2039e2043 2041
terms, only the determinations of constants (performance per unit determination of the residual glucose in the samples. We pro-
biomass and time under similar temperature and water conditions) ceeded using what is best described as a pulsed fed-batch soil
would allow the direct comparison of soil microbial activities of culture system. As shown in Fig. 1b soil samples received additional
different soils. The work described in our paper “Maintenance glucose-C amendments after a decrease of the stable CO2 response
carbon requirements of actively-metabolizing microbial pop- curve. Table 1. reproduces the results given in the original paper:
ulations under in situ conditions” (Anderson and Domsch, 1985a) we were fascinated by the fact that the carbon which was respired
was the first attempt to relate the CO2 output of the microbial per unit biomass (qCO2) reflected the amount of carbon needed per
community to the existing microbial biomass. We adopted Pirt’s unit biomass to maintain the previous level of CO2 evolution (the
(1975) term metabolic quotient, q, for the CO2 output per unit maintenance coefficient m). This meant that the C supplement
biomass, (qCO2) and here we describe the experiments since the provided the energy needed and which was oxidized totally to CO2
knowledge gained was the basis for much of our subsequent by catabolic processes at times where the growth rate equalled
research. Maintenance and eco-physiological quotients such as zero. The experimentally determined maintenance coefficients
growth rate (m), yield (Y), turnover time (d) (Anderson and Domsch, of the actively metabolizing biomasses of three soils ranged from
1986) and carbon uptake kinetics (Vmax, Km) (Anderson and Gray, 0.012 hÀ1 for two agricultural soils to 0.03 hÀ1 for one forest soil
1990) all had a big influence on the work which appeared in the and were in agreement with maintenance values from in vitro
three papers. single cell systems (background literature is given in Anderson and
The application of the substrate-induced respiration technique Domsch, 1985a) or extrapolated m values as cited above. Since the
for total microbial biomass determination with the use of the characteristic state of the major part of a total microbial community
“Ultragas 3 CO2-Analyzer (Anderson, 1982) allowed us to record the is dormancy and not anabolic activity, the next step for us was the
hourly CO2 production rates from the soil samples which had been determination of the m value of the dormant community.
initially spiked with glucose. We learned, when testing different We adopted the concept proposed by Sinclair and Topiwala (1970)
soils which had different levels of microbial biomass and by where maintenance “represented” a constant death rate of
applying increasing amounts of glucose, that CO2 output kinetics a culture. Viewed in this way, maintenance in an eco-physiological
were similar throughout the course of incubation: samples with an sense could be reduced to the question: how much carbon is
excess of glucose showed an increase in the rate of CO2 production necessary to maintain a constant level of microbial biomass? We
(due to cell proliferation) after the initial response maxima, while experimentally determined this in order to calculate m. Further, as
samples with an insufficient glucose supply remained below this stated above, the majority of the microbial community is dormant
initial response maxima. However, one particular glucose supply and as an approximation, the basal respiration (the CO2-C respired
induced a special type of CO2 response curve, where the CO2 efflux of the soil microbial biomass in a non-amended soil) should also
of the initial maximal response level did not change but instead reflect the maintenance energy needed. By calculating the qCO2
remained constant for several hours and then decreased (Fig. 1a). from the basal CO2 efflux rate it became evident that values for m
We assumed that this steady rate of CO2 production reflects the (obtained from the carbon rations supplied) where not equal to
energy demand for optimal metabolic activity (but not for growth) values for qCO2 as could be shown previously for the optimal
until the C source is depleted. This was confirmed by the concurrent carbon supplied and active microbial biomasses. Instead the carbon
released by CO2 (qCO2) was higher than the carbon needed to
maintain the biomass (m) (Anderson and Domsch, 1985b). The
conclusion drawn at that time was that in mainly dormant pop-
30 4000 ulations a large part of the “true m” must be met by endogenously
a
-1
1000 derived carbon sources. However, m values were up to two orders
µg CO 2-C g soil h
25 700 of magnitudes and qCO2 values one order of magnitude below
20 500 anabolically activated soil microbial communities; this verified
-1
control stable
15 a physiological difference between anabolic active and dormant
respiration
curve communities with respect to their maintenance carbon demand.
10 What emerged, in addition, was that both metabolic quotients
without glucose
5 responded with increases when the temperature was increased.
This indicated a higher energy demand. It was the beginning of our
0 systematic study of soil microbial communities and their response
0 2 4 6 8 10 12 14 16 18
to suboptimal conditions or environmental stress e such as soil
time (h)
20
-1
b
µg CO 2-C g-1 soil h
glucose added
Table 1
15 Comparison of metabolic quotients (q) for CO2 and the maintenance coefficient (m)
(see bold values).
10 Soils Ia II III
Biomass-C (mg gÀ1 soil) 147 Æ 6.1b 996 Æ 121 1982 Æ 32
5 Mean CO2-C rate (mg gÀ1 soil hÀ1) 1.83 Æ 0.004 12.7 Æ 0.4 25.2 Æ 0.12
Mean qCO2 (mg CO2-C mgÀ1 Cmic hÀ1) 0.0124 0.0127 0.0127
Glucose-C maintenance ration 1.82 12.7 61.8
0
0 2 4 6 8 10 12 14 16 18 (mg Cgluc gÀ1 soil hÀ1)
Mean CO2-C ratec (mg gÀ1 soil hÀ1) 1.85 Æ 0.007 12.9 Æ 0.10 25.0 Æ 0.13
time (h) Maintenance coefficient 0.0124 0.0127 0.031
(m) (mg Cgluc mgÀ1 Cmic hÀ1)
Fig. 1. (a) Example of a CO2 response curve of an arable soil (Chernozem) after
a
amendment with increasing concentrations of glucose. (b) Response of the microbial Soils I, II ¼ agricultural soils (Cambisol and Chernozem); soil III ¼ forest soil
population of the same soil to additional glucose-C amendments added after decrease (Rendzina).
b
of the stable CO2-C response rate. Arrows indicate time of additional glucose appli- ÆStandard deviation (SD); n ¼ 15.
c
cation. Figures are adapted from Figs. 1. and 4, Anderson and Domsch (1985a). Mean CO2-C rates after application of maintenance rations (as shown in Fig. 1b).

4. 2042 T.-H. Anderson, K.H. Domsch / Soil Biology & Biochemistry 42 (2010) 2039e2043
acidification. To quantify stress, we used the qCO2 of basal respi- significantly lower in the more complex beech-oak system than in
ration as an approximation of the true maintenance demand. pure beech stands (Anderson, 2009). We believe it confirms
our assumption of a development of a more efficient microbial
4. Determining soil microbial community differences using community in terrestrial systems with increasing diversity of
eco-physiological parameters organic matter input. Whether the observed differences of efficient
carbon use are attributed to greater species richness within the
The basis of two of our papers (Anderson and Domsch, 1989, microbial community remains an open question. This is a challenge
1990) rested on Odum’s (1969) theory on bioenergetics of to which we expect the molecular biologists to rise.
ecosystem development. This says that the development of diver- The metabolic quotient for CO2 (qCO2) has found world-wide
sity (plants, animals and microbes) in ecosystems coincides with an application in soil microbial ecology. It started with our former
increase of an efficient use of energy during the progress from colleague Heribert Insam (now at the University of Innsbruck)
a developmental stage to maturity and quasi-equilibrium and at who applied Odum’s theory on “bioenergetic economisation with
this point there is a low community respiration per unit biomass. successive age of an ecosystem” by studying soils of receding
When equilibrium is attained, input to any particular C compart- glaciers (Insam and Haselwandter, 1989) and our former colleagues
ment is equal to output, and there is no further accumulation or Andreas Fließbach, Rainer Martens, Hans Reber, using the qCO2 as
reduction of organic matter in that compartment. Extrapolated to an stress indicator of soils contaminated with heavy metals
soils and the microbial biomass compartment, this would mean (Fließbach et al., 1994). Further, the qCO2 and the Cmic-to-Corg ratio
that at maturity there should be a low microbial community were implemented as soil microbial parameters in the continuous
respiration per unit microbial biomass (qCO2) and a high microbial observation programme of 90 soil sites in Lower Saxony, Germany,
biomass supported per unit energy source (C-source), which would 1991 (Höper and Kleefisch, 2001).
be reflected in a high ratio of biomass-C-to-total organic C (the
Cmic:Corg ratio). Since Odum’s theory also encompasses the diver-
sity of substrate litter inputs from the primary producer to the soil 5. Some concluding remarks
system, we assumed that agricultural long-term permanent
monoculture soils (M) could be considered as less diverse in litter We look back with some pride on the large number of publica-
input in comparison to long-term continuous crop rotation plots tions where metabolic quotients, particular the specific respiration,
(CR). After analysis of over 100 plots with a long-term management qCO2, have been applied for the quantification of environmental
history (at least 15 years to approximate a quasi-equilibrium state) effects on the microbial community in soils. And we still believe that
from 26 sites at different locations in Europe, we were able to show metabolic quotients have a great and as yet unrealised potential for
that these two management systems differed: mean % Cmic in Corg improving our understanding of the development of microbial
for M soils was to 2.3 and for CR soil 2.9; this coincided with almost communities in the ecosystem that they inhabit. Unfortunately,
twice the value for qCO2 for M plots as compared to CR plots. Since now and then, the relative ease of their determination leads to
these differences were not related to soil texture or pH, the misapplication. For example, a high qCO2 is sometimes explained
assumption made was that the different management practices with a high microbial activity and is interpreted as a positive
(monoculture as opposed to crop rotation), must have determined property. In ecological terms, however, a high qCO2 reflects a high
the different energy demands of the microbial pools. It became maintenance carbon demand, and if the soil system cannot
clear to us that we should repeat this analysis by investigating replenish the carbon which is lost through respiration, microbial
natural soil systems. As we were involved in forest ecosystem biomass must decline. Also, care must be taken how and when basal
research projects at the University of Göttingen at that time, we had respiration is determined. In our publications on metabolic
the opportunity to study forest stands with different litter inputs, quotients we have discussed the fact that we are dealing with
comparing simple systems of beech monocultures with mixed physiological quotients (Anderson, 1994). With respect to the
beech-oak stands over a long-term period. The paper which is microbial biomass in soil, we know that it is not static over the year.
the third in the sequence (Anderson and Domsch, 1993) reports on It undergoes many changes, including those in its physiological
the effects of soil pH on the microbial biomass which emerged status. The specific respiration, qCO2, will be particularly affected,
after the study of over 100 forest stands. The pH effect was since the CO2 efflux for its calculation rests on the ratio of the
so pronounced in showing an increased qCO2 and a decreased Cmic- growing to dormant portion of cells. Here, although self-evident, it
to-Corg ratio under acidic conditions in comparison to neutral is of paramount importance that the time (e.g., season) of sampling
stands, that we assumed that we had found a microbial community is comparable if physiological comparisons are to be made.
stress indicator in the sense of Odum (1985) who commented The holistic approach which we pursued was necessary at that
“repairing damage by disturbances requires diverting energy from time to understand the relationship between soil microbial
growth and production to maintenance”. To pursue our original biomass its energy transfer and carbon demand. To us, the detec-
goal: the comparison of pure beech stands to mixed beech-oak tion of an energy economy at the microbial biomass level, together
stands, we had to search for stands with comparable pH and age. with an increase in the diversity of litter input, was really exiting.
This screening went on for years and was finally completed and What the physiological quotients could not provide was direct
the data analysed in 1998 after studying of over 1000 stands. proof of a greater species diversity in such soil systems. For
The findings of this extensive investigation were published recently a decade now, the possible linkage between above-ground biodi-
in a collaborative book project (Brumme and Khanna, 2009). versity as a controlling factor of below-ground species diversity has
We could, indeed, show that the more complex beech-oak stands become a research issue (e.g., Wall and Moore, 1999; Hooper et al.,
had a higher percent Cmic in Corg than that of pure beech stands 2000; Wardle et al., 2004). At least for the time being the emphasis
which suggested a more efficient use of the available carbon by the lies on descriptive techniques such as BiologÒ, phospholipids fatty
beech-oak microflora. For mature beech-oak stands on neutral soils acid (PLFA) or DNA analyses for determining the microbial
the mean percent Cmic in Corg was 2.7 and for the pure beech stands community structure. We believe a combination of a holistic
2.3 which, coincidentally, are similar values to those found for approach (e.g., metabolic quotients) and specific molecular tech-
agricultural soil systems (see above). On the other hand, the unit niques for testing whether microbial diversity is related to
respiration released per unit microbial biomass, the qCO2, was a microbial communities` energy economy could open a new

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