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Applied and Environmental Microbiology, September 2000, p. 3878-3882, Vol. 66, No. 9
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Ethylene Removal at Low Temperatures under
Biofilter and Batch Conditions
Lars
Elsgaard*
Danish Institute of Agricultural Sciences,
Department of Crop Physiology and Soil Science, Research Center
Foulum, DK-8830 Tjele, Denmark
Received 19 May 2000/Accepted 2 July 2000
 |
ABSTRACT |
Removal of the plant hormone ethylene
(C2H4) is often required by horticultural
storage facilities, which are operated at temperatures below 10°C.
The aim of this study was to demonstrate an efficient, biological
C2H4 removal under such low-temperature conditions. Peat-soil, acclimated to degradation of
C2H4, was packed in a biofilter (687 cm3) and subjected to an airflow (~73 ml
min
1) with 2 ppm (µl liter1)
C2H4. The C2H4 removal
efficiencies achieved at 20, 10, and 5°C, respectively, were 99.0, 98.8, and 98.4%. This corresponded to C2H4
levels of 0.022 to 0.032 ppm in the biofilter outlet air. At 2°C, the
average C2H4 removal efficiency dropped to
83%. The detailed temperature response of C2H4
removal was tested under batch conditions by incubation of 1-g soil
samples in a temperature gradient ranging from 0 to 29°C with
increments of 1°C. The C2H4 removal rate was
highest at 26°C (0.85 µg of C2H4 g [dry
weight]1 h1), but remained at levels of
0.14 to 0.28 µg of C2H4 g (dry
weight)1 h1 at 0 to 10°C. At 35 to
40°C, the C2H4 removal rate was negligible (0.02 to 0.06 µg of C2H4 g [dry
weight]1 h1). The
Q10 (i.e., the ratio of rates 10°C apart) for
C2H4 removal was 1.9 for the interval 0 to
10°C. In conclusion, the present results demonstrated microbial
C2H4 removal, which proceeded at 0 to 2°C and
produced a moderately psychrophilic temperature response.
| |
INTRODUCTION |
The alkene
C2H4 (common name, ethylene; International
Union of Pure and Applied Chemistry name, ethene) is unique among
atmosphere-polluting hydrocarbons because it is a plant hormone.
Biological effects of C2H4 occur at
concentrations below 0.1 ppm, which is generally more than 100-fold
lower than those for other short-chain hydrocarbons (13).
Air purification by biological filters (20) has been
suggested as a method of C2H4 removal from
industrial waste gas and from horticultural storage facilities, where
plant-produced C2H4 may accumulate to levels
that cause a premature ripening or senescence of the plant material
(2, 6, 7, 8, 10, 29, 30). During storage and transport of
horticultural produce, temperatures below 10°C are often obligatory;
for instance, 4 to 6°C is optimal for 35% (and acceptable for 85%)
of the transport volume of potted plants produced in Denmark
(17). A prerequisite for successful biofiltration under such
conditions is the existence of C2H4-degrading microorganisms with sufficient activity at low temperatures. So far,
however, biocatalysts for efficient C2H4
removal at temperatures below 10°C have not been described.
In the present report, microbial C2H4 removal
at temperatures as low as 0 to 2°C was shown to occur indigenously in
horticultural peat-soil under biofilter and batch conditions.
| |
MATERIALS AND METHODS |
Acclimated peat-soil.
Horticultural peat-soil (Pindstrup
Blend 2; Pindstrup Mosebrug, Pindstrup, Denmark) was acclimated to
C2H4 degradation by incubation of 800 g of
soil (185 g [dry weight]) in a gastight glass bottle (5.5 liters)
with a headspace concentration of ~500 ppm
C2H4. Through a butyl rubber stopper, gas
samples (0.5 ml) for C2H4 analysis were
withdrawn regularly during incubation at room temperature (~20°C)
for 28 days. After depletion of the C2H4, the
bottle was purged with atmospheric air and new
C2H4 was added. This was done repeatedly (six
times) upon subsequent depletions.
Biofilter experiment.
A biofilter was made from an acrylic
core (inner diameter, 5 cm; effective length, 35 cm) as previously
described (10). Acclimated peat-soil was packed in the
biofilter (~0.15 g [dry weight] cm3), and a
humidified mixture of atmospheric air and 10 ppm
C2H4 (4:1) was supplied to the inlet of the
biofilter by two mass flow controllers (10). The flow rate
(~73 ml min1) was verified daily with a digital
flowmeter at the biofilter outlet. The biofilter was first operated at
room temperature (~20°C) and then at 10, 5, and 2°C in a
thermostatted incubator (Refritherm 6E; Struers, Rødovre, Denmark).
During operation at 2°C (and 5 and 10°C in control experiments),
temperatures at biofilter soil depths of 5 and 25 cm (i.e., distances
from the inlet) were measured with permanently installed thermometers
with steel penetration probes. During operation for 20 days, gas
samples (20 ml) for C2H4 analysis were
regularly collected. Thus, at each of 36 sampling occasions, the
C2H4 removal efficiency was determined from
three pairs of inlet (Cin) and outlet (Cout)
C2H4 concentrations (removal efficiency = [1 
Cout/Cin] × 100%). Additional
gas samples (duplicates) were collected through butyl rubber stoppers
at biofilter soil depths of 5, 10, 15, 20, 25, and 30 cm.
Temperature gradient batch experiments.
Peat-soil from the
biofilter was sieved (2 mm; final dry matter content, 18.7%) and
weighed (1 g) portions were placed into 90 test tubes (28 ml), which
were closed with butyl rubber stoppers and crimp seals. Triplicate test
tubes were equilibrated (1 to 2 h) at each of 30 different
temperatures, ranging from 0 to 29°C, in a temperature gradient
incubator. Basically, this device was an insulated aluminum bar with 30 rows of six sample wells that fit the 28-ml test tubes. Cooling and
heating were applied (and automatically regulated) at opposite ends of
the aluminum bar, thereby producing a thermal gradient with increments
of 1°C. The temperatures of 15 sample rows in the aluminum bar were
measured by permanently installed Pt-100 sensors, and the recordings
were logged on a personal computer at 5-min intervals. Temperatures of
intermediate sample rows were calculated by linear regression.
After temperature equilibration, each test tube was injected with
C2H4 to an initial headspace concentration of
~500 ppm (511 ± 14 ppm; mean ± standard deviation;
n = 30). Over a time course of 3 to 7 days, the
C2H4 concentration in each test tube was
measured four to six times, and the rates of
C2H4 removal were calculated by linear regression.
By using the same approach described above, the
C
2H
4 removal rates at 25, 35, and 40°C were
tested with biofilter soil samples
that had been stored at 2°C and
reacclimated (15°C) under a headspace
of ~500 ppm
C
2H
4.
Fate of C2H4.
The transformation of
C2H4 to CO2 was tested with
acclimated peat-soil (4 g) incubated in stoppered 120-ml serum bottles
with or without ~750 ppm C2H4. For each
treatment (i.e., with or without C2H4), three
soil samples were incubated at 5 and 15°C. Gas samples (0.2 ml) for
analysis of C2H4 and CO2 were
withdrawn during incubation for 2 weeks.
Analyses and statistics.
C2H4 was
quantified with a Shimadzu GC-14B gas chromatograph with a flame
ionization detector. Gases were separated on a Poropak Q (100 to 120 mesh) steel column (inner diameter, 2 mm; length, 1.9 m) at
95°C. The injection and detection temperatures were 150 and 200°C,
respectively. During the biofilter experiments, gas samples were
injected through a 2.5-ml sample loop that was purged with a sample
volume of 20 ml. With this configuration, the
C2H4 detection limit was 0.013 ppm for a
signal/noise ratio of 3. During the remaining experiments, gas samples
(0.5 ml) were injected directly by using a 1-ml gastight syringe.
CO
2 was quantified with a GC 82 gas chromatograph
(Mikrolab, Højbjerg, Denmark) with a temperature conductivity
detector.
The column (Poropak N) was operated at 60°C with He as the
carrier
gas (flow rate, 43 ml min
1). The injected sample
volumes were 0.2 to 0.5
ml.
Dry matter content was determined gravimetrically after drying of three
to six soil samples overnight at 105°C. Soil pH was
measured by a
glass electrode in soil-water suspensions (1:5).
Unless otherwise stated, the results of replicate samples are presented
as means ± standard deviations for the number of samples
(
n)
indicated.
| |
RESULTS |
Acclimated peat-soil.
Degradation of
C2H4 was initially preceded by an acclimation
period of ~11 days, and thereafter, the C2H4
pool was depleted within 6 days (data not shown). New
C2H4 was depleted within 1 to 2 days with no
further acclimation period. After the last C2H4 addition, the rate of headspace C2H4 removal
(HR) was 36 ppm h1 (data not shown). For the
headspace volume (V) of ~5 liters and the soil content
(M) of 185 g (dry weight), this corresponded to a
specific removal rate (SR) of 1.13 µg of
C2H4 g (dry weight)1
h1 as calculated by SR = HR × V ×
(C2H4) × M1,
where (C2H4) is the density of
C2H4 at 20°C (1.16 µg µl1).
Biofilter experiment.
During the biofilter experiment (20 days), the flow rate ranged from 72.0 to 73.4 ml min1
(73.0 ± 0.4 ml min1; n = 23). The
inlet C2H4 concentration ranged from 1.92 to
2.13 ppm (2.01 ± 0.05 ppm; n = 36). The soil pHs
before and after the biofilter experiment were 5.7 ± 0.1 and
5.9 ± 0.1, respectively (n = 6).
Measurements of the outlet C
2H
4 concentration
after 0.5 h of operation showed that 82.0% of the incoming
C
2H
4 was initially
removed (Fig.
1). After 2 days of operation, the
efficiency of
C
2H
4 removal increased to 99.0% ± 0.2% (
n = 4). Hence, during
operation for 2 to 6 days at 20°C, the biofilter had an outlet
concentration of only
0.022 ± 0.005 ppm C
2H
4 (
n = 4). When the
biofilter was transferred from 20 to 10°C, no
significant change
in the C
2H
4 removal
efficiency (98.8% ± 0.6%;
n = 6) occurred
during
operation for 2 days (Fig.
1). Lowering the incubation
temperature to
5°C caused a transient decrease in the C
2H
4
removal
efficiency to 95.0%. Then, during operation for 3 to 6 days at
5°C, the removal efficiency increased to 98.4% ± 0.5%
(
n = 5),
with an average outlet
C
2H
4 concentration of 0.032 ± 0.010 ppm
(
n = 5). Further lowering of the incubation temperature
to 2°C
caused a permanent decrease in the average removal efficiency
to 83.0% during 6 days of operation (Fig.
1). This corresponded
to an
outlet C
2H
4 level of 0.338 ± 0.030 ppm
(
n = 13).
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FIG. 1.
C2H4 removal efficiency of the
biofilter during operation at 20, 10, 5, and 2°C with 2 ppm
C2H4. The dotted lines indicate the temperature
transitions. The data represent the mean of three determinations.
Coefficients of variation ranged from 0 to 3%. Note the y
axis starts at 80%.
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|
C
2H
4 measurements at different biofilter soil
depths showed that all soil layers were initially exposed to
C
2H
4 levels declining
from 2.03 ppm at the
inlet (i.e., 0-cm soil depth) to 0.37 ppm
at the outlet (i.e., 35-cm
soil depth). However, after 5 days
of operation at 20°C, the
C
2H
4 removal occurred almost completely
within
the first 0 to 10 cm of the biofilter (Fig.
2). Similarly,
after 5 days of operation
at 5 and 2°C, the C
2H
4 removal occurred
within the first 0 to 15 cm of the biofilter (Fig.
2). At 2°C,
however, a relatively high C
2H
4 concentration
(~0.34 ppm) passed
through the 15- to 35-cm soil layer without
further removal (Fig.
2).
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FIG. 2.
C2H4 concentrations at different
biofilter soil depths after operation for 5 days at 20°C ( ), 5°C
( ), and 2°C ( ). Soil depths of 0 and 35 cm represent the
biofilter inlet and outlet, respectively.
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|
The temperatures measured in the center of the biofilter during
operation at 2°C (6 days) were 2.7 ± 0.3°C at a 5-cm soil
depth and 1.8 ± 0.3°C at a 25-cm soil depth (
n = 18). Control
experiments showed that incubation of the biofilter
at 10°C resulted
in constant temperatures of 10.4 and 9.9°C at soil
depths of 5
and 25 cm, respectively. During control incubation at
5°C, the
temperature of the inlet gas was 6.1°C, and constant
temperatures
of 5.3 and 4.9°C were measured at soil depths of 5 and
25 cm,
respectively.
Temperature gradient batch experiments.
Table
1 shows the highly constant incubation
temperatures in the thermal gradient during the batch incubation period
of 7 days. Linear regression between the temperature and the sample row
position (y = 1.00x + 30.13) had a regression
coefficient (r2) of 1.000 (n = 15).
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TABLE 1.
Mean, minimum, and maximum temperatures for individual
sample rows during a 7-day temperature gradient incubation
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|
A linear time course of C
2H
4 removal was
observed at all temperatures during the temperature gradient
incubation. Linear regression
coefficients
(
r2) ranged from 0.84 to 1.00, with a
mean of 0.98 (
n = 90). The
highest
C
2H
4 removal rate (0.85 µg of
C
2H
4 g [dry weight]
1
h
1) occurred at 26°C (Fig.
3). At lower temperatures, the
C
2H
4 removal
rate decreased, but remained
at levels of 0.14 to 0.28 µg of C
2H
4 g (dry
weight)
1 h
1, even at 0 to 10°C (Fig.
3).
For soil samples incubated at 25,
35, and 40°C (after storage and
reacclimation), the C
2H
4 removal
rates were
0.72 ± 0.02, 0.06 ± 0.03, and 0.02 ± 0.01 µg of
C
2H
4 g (dry weight)
1
h
1, respectively (
n = 3).
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FIG. 3.
Temperature dependence of C2H4
removal in batch incubations of biofilter soil. The data represent the
mean ± standard error (n = 3). The insert shows
an Arrhenius plot with linear regression of data below the optimum
temperature ( 26°C).
|
|
Below the optimum temperature of 26°C, the temperature
dependence of C
2H
4 removal fitted the
Arrhenius equation: ln (rate)
= ln
A +
Ea/
RT, where
A is a constant,
Ea is the apparent activation
energy,
R is the gas constant, and
T is the absolute
temperature
(
3). From the slope of the Arrhenius plot (Fig.
3, insert),
Ea was found to 45 kJ
mol
1. This
Ea corresponded to a
Q10 of 1.9, as calculated for the
temperature
interval from 0 to 10°C {
Q10 = exp[
Ea × 10/
RT × (
T + 10)]}.
Fate of C2H4.
In batch experiments at
15°C, added C2H4 (equivalent to 3.7 ± 0.1 µmol; n = 3) was depleted in 4 days with a
concurrent CO2 production of 34.1 ± 2.8 µmol of
CO2 (n = 3). In samples without added
C2H4, the CO2 production was
27.5 ± 3.2 µmol of CO2 (n = 3).
Thus, on average, the additional CO2 production in samples with C2H4 was equivalent to 6.6 µmol of
CO2. At 5°C, added C2H4 (equivalent to 3.7 ± 0.1 µmol of C2H4)
was depleted after 12 days with a concurrent CO2 production
of 25.0 ± 2.0 µmol of CO2 (n = 3).
In samples without added C2H4, the
CO2 production corresponded to 22.8 ± 0.8 µmol of
CO2. Thus, the additional CO2 production in
samples with C2H4 was equivalent to 2.2 µmol
of CO2.
| |
DISCUSSION |
C2H4 removal by soil samples was first
reported by Abeles et al. (1) and has been documented by
several authors (5, 26, 27, 35). The process is mainly
mediated by ethylene-degrading bacteria, which have been isolated from
various soil types (5, 16, 24, 31). Thus, the capacity for
C2H4 degradation has been found in such genera
as Xanthobacter, Nocardia,
Mycobacterium, Rhodococcus, Bacillus,
and Pseudomonas (25, 31). In some soil types,
including the present peat-soil, an acclimation period of several days
to weeks may precede the C2H4 removal (5,
11). This is most likely explained by enzyme activation or growth
of the ethylene-degrading bacteria, which initially may occur in low
numbers (5, 34). Indeed, the microbiological nature of the
C2H4 removal in the present experiments was
demonstrated by the initial acclimation period of ~11 days, which
disappeared for subsequent additions of C2H4.
Also, the microbial mediation of the C2H4
removal was suggested from the close association of optimum (26°C)
and maximum (35 to 40°C) temperatures, which are characteristic of
enzymatic processes. Finally, in batch experiments with the present
peat-soil type, it was shown that no C2H4
removal occurred when the peat-soil was sterilized by autoclaving on 2 consecutive days prior to incubation (data not shown).
C2H4 removal by biofilters.
C2H4 removal by inoculated biofilters (for
examples, see references 7 and
29) has been surveyed previously (10,
11). However, a comparison of different filters is difficult or
even impossible unless they have been operated under exactly the same conditions (e.g., inlet C2H4 concentration and
volume/flow ratio). The present biofilter was operated under similar
conditions to a peat-soil biofilter, which was inoculated with
ethylene-oxidizing bacteria (10). This allowed a comparison
of acclimated peat-soil and inoculated peat-soil as biofilter
materials. The present biofilter showed a lowest outlet level of 0.022 ppm of C2H4 within few days of operation at
20°C. This was similar to the lowest outlet concentration (0.017 to
0.020 ppm C2H4) observed for the inoculated
biofilter (10). Also, it was shown that
C2H4 removal occurred primarily within the
first 10-cm soil segment of each of the biofilters. Thus, a similar
removal efficiency apparently could be obtained with acclimated and
inoculated peat-soil under biofilter conditions with 2 ppm
C2H4. For experiments with much higher loads of
C2H4 (inlet concentration of ~117 ppm
C2H4), both biofilter types also showed an
efficient C2H4 removal, but differed in
operational stability, which was highest for the inoculated biofilter
(10, 12).
Using a biofilter based on indigenous microorganisms in compost, van
Ginkel et al. (
30) showed that C
2H
4
removal was induced
after ca. 4 weeks of operation with 2 ppm
C
2H
4 (flow rate, 1.3
ml min
1;
reactor volume, 15 cm
3; temperature, 30°C). At the end of
an 8-week operation period,
the C
2H
4 removal
efficiency corresponded to ~45%, but a stable
(and maximal)
efficiency was not attained during the experiment
(
30).
Therefore, a comparison between the acclimated compost
biofilter and
the present peat-soil biofilter was not
possible.
Temperature dependence of C2H4
removal.
The effect of low temperature on
C2H4 removal has only been tested in few
studies. Thus, van Ginkel et al. (29) concluded that
C2H4 removal by liquid cultures of a known
biocatalyst, Mycobacterium sp. strain E3, declined rapidly
below 10°C and was almost absent at 4°C. Also, de Bont
(5) found that no appreciable C2H4
removal occurred when a clay soil was incubated at 4°C, and,
likewise, forest soil samples removed almost no
C2H4 when incubated at 0 and 10°C
(25). A 1998 study (10) showed that an inoculated biofilter could be adapted to efficient C2H4
removal at 10°C, but the performance at lower temperatures was not
tested. The present study for the first time has demonstrated microbial
C2H4 removal at temperatures as low as 0 to
2°C. Furthermore, the increase in C2H4
removal efficiency that occurred during biofilter operation at 5°C
indicated adaptation (or possibly growth) of ethylene-degrading microorganisms at this temperature (Fig. 1).
C
2H
4 removal by indigenous microorganisms in
peat-soil in principle could be mediated by different groups of
microorganisms
with different temperature responses. However, the
present data
did not reveal the occurrence of such different
temperature groups,
because only one temperature optimum was identified
from the fine-scale
temperature response of
C
2H
4 removal. Thus, the activated peat-soil
seemed to be dominated by only one group of ethylene-degrading
bacteria
or, alternatively, by different groups with similar temperature
responses. The present temperature response was characterized
by a
relatively low
Q10 of 1.9, which was in
accordance with low
temperature sensitivity and consequently a
relatively high rate
at low temperature (
23).
Microbial temperature groups.
Although no categorical
definitions exist (for examples, see references 4, 14,
18, and 33), microorganisms may be divided
into thermal groups, such as psychrophiles and mesophiles, based on
minimum, optimum, and maximum temperatures for growth (Tmin, Topt, and
Tmax, respectively). Organisms which are not truly psychrophilic (21), but still able to grow at 5°C,
may be considered as psychrotrophs or (more correctly) moderate
psychrophiles (9; H. W. Jannasch, Letter, ASM
News 64:185, 1998). A current definition of this group was adopted by
Wiegel (33), who used the criteria
Tmin <5°C, Topt
>15°C, and Tmax >20°C.
While the definitions of thermal groups apply to microbial growth
temperatures, the same terminology is often used to characterize
the
temperature dependence of metabolic processes, such as respiration
or
substrate degradation. Growth and metabolic rates may not scale
directly (
22,
32), however, and therefore the growth
response
of the present microorganisms was uncertain, although the
temperature
response of microbial C
2H
4
degradation could be characterized
as moderately psychrophilic.
However, a moderately psychrophilic
growth response could not be
excluded, because the
Topt and
Tmax for growth may actually be lower than those
for metabolic processes
in cold-adapted bacteria (
15,
18,
19,
28).
Fate of C2H4.
Based on the
relationship between C2H4 removal and
CO2 accumulation, an attempt was made to determine the fate
of C2H4 in the acclimated peat-soil. At 15°C,
removal of 3.7 µmol of C2H4 was accompanied
by increased production of CO2 (equivalent to 6.6 µmol).
These data were in reasonable agreement with the following stoichiometry of complete C2H4 oxidation:
At 5°C, removal of 3.7 µmol of C
2H
4
was accompanied by increased CO
2 production (equivalent to
2.2 µmol). Rather than a complete
C
2H
4
oxidation to CO
2, these data indicated the accumulation of
intermediate products during the C
2H
4
depletion. However, no gaseous
intermediates were detected during the
experiments, and therefore
the existence of intermediates was not
confirmed. Indeed, the
peat-soil system may not be ideal for mass
balance studies due
to the abundance of organic carbon substrates.
Thus, it cannot
be excluded that ethylene-oxidizing bacteria may shift
from utilization
of C
2H
4 to other carbon
substrates when C
2H
4 is not available.
Therefore, an apparent lack of CO
2 production in response
to C
2H
4 removal may be caused by a higher
CO
2 production from other carbon
substrates in the absence
of C
2H
4 rather than in its presence.
In
conclusion, the present C
2H
4 removal was
mediated by ethylene-oxidizing
microorganisms, which at least at 15°C
caused a complete oxidation
of C
2H
4 to
CO
2.
| |
ACKNOWLEDGMENTS |
Excellent laboratory assistance from Gitte Hastrup Andersen and
helpful comments from Bo Thamdrup and two anonymous reviewers are
greatly acknowledged.
| |
FOOTNOTES |
*
Mailing address: Danish Institute of Agricultural
Sciences, Department of Crop Physiology and Soil Science, Research
Center Foulum, P.O. Box 50, DK-8830 Tjele, Denmark. Phone: 45 8999 1873. Fax: 45 8999 1619. E-mail:
lars.elsgaard{at}agrsci.dk.
| |
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Applied and Environmental Microbiology, September 2000, p. 3878-3882, Vol. 66, No. 9
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
