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Applied and Environmental Microbiology, September 2000, p. 4050-4057, Vol. 66, No. 9
Department of Civil and Environmental
Engineering,1 Center for Microbial
Ecology,2 and Department of
Microbiology,3 Michigan State University,
East Lansing, Michigan 48824, and EFX Systems, Lansing,
Michigan 489104
Received 2 February 2000/Accepted 29 May 2000
Parallel processing is more stable than serial processing in many
areas that employ interconnected activities. This hypothesis was tested
for microbial community function using two quadruplicate sets of
methanogenic communities, each set having substantially different
populations. The two communities were maintained at a mean cell
residence time of 16 days and a mean glucose loading rate of 0.34 g/liter-day in variable-volume reactors. To test stability to
perturbation, they were subjected to an instantaneous glucose pulse
that resulted in a 6.8-g/liter reactor concentration. The pattern of
accumulated products in response to the perturbation was analyzed for
various measures of functional stability, including resistance,
resilience, and reactivity for each product. A new stability parameter,
"moment of amplification envelope," was used to compare the soluble
compound stability. These parameters indicated that the communities
with predominantly parallel substrate processing were functionally more
stable in response to the perturbation than the communities with
predominantly serial substrate processing. The data also indicated that
there was good replication of function under perturbed conditions; the
degrees of replication were 0.79 and 0.83 for the two test communities.
Parallel processing of complex
interconnected activities has been proven to be a more efficient and
robust approach in many systems, including information processing
(5, 13), fluid flow (7), neurobiology
(10), and communication (5). This phenomenon may
also hold true for mixed microbial systems since functionally they are
also equivalent to a network of metabolic activities of many
interdependent populations. Methanogenic systems are good examples of
networks in which a number of fermentative, syntrophic, and
methanogenic populations work together as a community to convert
organic substrates to methane via the well-recognized anaerobic
food chain (Fig. 1a). If the above
hypothesis is true, a substrate perturbation processed through
multiple routes in parallel should result in a higher functional
stability of the system because of the potential distribution of
substrate to several populations or activities. Alternatively, if the
same perturbation is processed through routes involving a smaller
number of intermediate products in a serial manner, then the system
should be less stable. The kinetic and thermodynamic constraints on
each route may, in addition, modulate the outcome. Several issues
emerge at the outset for testing such a hypothesis; these issues
include establishment of the two systems, quantification of the
functional stability, and replication of results. We address these
issues as follows.
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Parallel Processing of Substrate Correlates with Greater
Functional Stability in Methanogenic Bioreactor Communities
Perturbed by Glucose
ABSTRACT
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Abstract
Introduction
Materials and Methods
Results and Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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FIG. 1.
Anaerobic food chain as a network of substrate flow
through a methanogenic community (a) and ecological parameters
of functional stability (b).
Performance of the same overall function by different microbial communities under the referential state is perhaps ubiquitous. However, selecting two communities that perform the same overall function (viz., conversion of complex organic substrate to methane) via parallel and serial routes in both referential and perturbed states is extremely difficult, if not impossible, with our current knowledge of microbial systems. To approximate the processing differences, we used two methanogenic communities that originated from anaerobic digestor sludge from the same wastewater treatment plant but differed widely in their maintenance periods on glucose as well as in their dominant fermentative and methanogenic populations (4). One inoculum source was operated for 17.5 mean cell residence times (MCRTs), and the other was operated only for 5.8 MCRTs before a substrate perturbation was applied. Based on these differences, we expected that the two communities would also differ in their responses to the perturbation. Whether they would conform to the parallel or serial model of substrate flow under the perturbed conditions was not known a priori.
To measure functional stability, we adopted parameters described in ecology (6, 11) in terms of the amplification envelope of key intermediate products in response to a perturbation (Fig. 1b). The two main parameters obtained from this envelope are resistance and resilience. Resistance of a community with respect to an intermediate product is defined as the maximum accumulation of the product. It is a measure of the buffering capacity of the community with respect to the corresponding intermediate product (11). Resilience is defined as the time taken by the accumulated intermediate product to return to its referential state (11). As defined, a higher numerical value denotes lower resistance or resilience. A third component of the amplification envelope that may be useful in characterizing the stability is reactivity, which is defined by the maximum slope of the rising limb of the envelope (11).
For replication, we used four identical reactors for each inoculum source. Replication was an important part of this study because it is possible that two communities similar in function under a referential state may perform quite differently under perturbed conditions. This may be due to underlying differences that may exist in the microbial community structure or in the biochemical pathways that are operating in the two communities. It was anticipated, however, that multiple communities originating from the same source and maintained under identical conditions without contamination should be similar with respect to function under both referential state and perturbed conditions.
The responses of the two communities to the applied perturbation indicated that their functional stabilities were related to the substrate flow pattern. We observed greater stability in the communities that processed glucose by parallel pathways. In addition, the functional responses of the two communities were found to be replicable within each set under perturbed conditions.
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MATERIALS AND METHODS |
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Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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Reactor operation, inoculum source, and characteristics. Two sets of variable-volume methanogenic reactors were operated with an effective MCRT of 16 days. One set, designated the high-spirochete (HS) set (reactors 5 through 8), was dominated by spirochetes, short rods, and methanosarcinas (4), and the other set, designated the low-spirochete (LS) set (reactors 1 through 4), was dominated by cocci and methanosaetas. Each reactor consisted of a 500-ml reagent bottle (Fisher Scientific, Pittsburg, Pa.) sealed with a butyl rubber stopper (Fisher Scientific) and maintained at 35°C in a temperature-controlled water bath (Lab Line Instruments, Inc., Melrose Park, Ill.). Reactor contents were completely mixed with stir bars and were protected from light. Feeding and sampling ports for the liquid and headspace were made by using 2- to 6-in.-long 18-gauge syringe needles (Fisher Scientific), 3/8-in.-diameter tubing (low O2 permeability; Cole Parmer Instrument Co., Vernon Hills, Ill.), and plastic connectors and valves (Cole Parmer). A sterile glucose solution (8 g of glucose per liter, 7 g of sodium bicarbonate per liter) and a sterile nutrient solution (40× diluted) (16) were fed at rates of 12.5 and 5 ml/day, respectively, by using 140-ml syringes (Sherwood Medical Co., Norfolk, Nebr.) and syringe pumps (Harvard Apparatus, Inc., Holliston, Mass.). A 3.5-ml sample of each suspended culture was removed daily for measurement of pH, optical density, and soluble intermediate products.
After a period of 8 days, the 112 ml of suspended culture that accumulated was removed from each reactor and used for substrate utilization and community characterization assays. As a result, the liquid volume of the reactors varied from 250 to 362 ml over a period of 8 days (causing the glucose loading rate to cycle between 0.40 and 0.28 g/liter-day over an 8-day period). This sampling and wasting schedule resulted in an MCRT of 16 days. Each wasted volume was replaced by an equivalent volume of an oxygen-free CO2-N2 (50:50) gas mixture from a 4-liter Tedlar gas collection bag (Cole Parmer) that was filled immediately prior to wasting. These bags were also used to collect the gases produced over the 8-day period and to provide replacement gas for daily sampling. The source and purity of all chemicals used in this study for feeding or standardization were the same as those described previously (16). Inocula for both sets of reactors were obtained from two 18-liter mother reactors fed glucose and seeded with anaerobic digester sludge from the municipal wastewater treatment facility at Jackson, Mich. The mother reactor for the HS set operated for more than 4 years under two different operating conditions. For the first 3.5 years, it operated at a loading rate of 0.8 g/liter-day and at an MCRT of 10 days. Nearly 200 days prior to its use as the inoculum source for the HS set, it received additional anaerobic digester sludge from the same source and was switched to a loading rate of 0.5 g/liter-day and an MCRT of 16 days. The mother reactor for the LS set was operated for 60 days at an MCRT of 16 days and at a loading rate of 0.5 g/liter-day. At the time of inoculation of the two sets of reactors, the soluble organic carbon removal efficiency measured by chemical oxygen demand (COD) for both mother reactors was greater than 90%. The maximum substrate utilization rates for the mother reactor of the HS set were 29.1 ± 3.2 µmol/mg of protein/h for glucose, 7.6 ± 3.3 µmol/mg of protein/h for lactate, 2.5 ± 0.45 µmol/mg of protein/h for acetate, and 0.92 ± 0.18 µmol/mg of protein/h for butyrate. For hydrogen, the maximum substrate utilization rate, measured as the rate of production of CH4, was 11.4 ± 4.6 µmol/mg of protein/h. A methanogenic inhibition assay performed with bromoethanesulfonic acid (12) indicated that at 1 mM glucose fed in batch, the mother reactor for the HS set accumulated mostly acetate while the mother reactor for the LS set accumulated both acetate and butyrate.Analytical techniques and assays.
The efficiency of soluble
organic carbon removal was monitored by analyzing COD and intermediate
soluble products, including acetate, butyrate, isobutyrate, propionate,
formate, lactate, and ethanol. Cells were removed by centrifugation at
6,000 × g for 15 min, and an appropriate amount of the
supernatant fluid was digested for COD analysis by using Hach 0- to
1,500-ppm-range COD vials (Hach Company, Loveland, Colo.). Glucose and
soluble intermediate products were analyzed with a high-performance
liquid chromatograph (HPLC) equipped with a 300-mm HPX-87H ion
exclusion column (Bio-Rad Laboratories, Hercules, Calif.) connected to
a UV/Vis absorbance detector (Shimadzu, Wood Dale, Ill.) set at 210 nm
and a refractive index detector (Waters, Inc., Milford, Mass.). The
mobile phase was 0.013 N H2SO4 at a flow rate
of 0.7 ml/min, and the column temperature was set at 65°C.
Centrifuged reactor samples were filtered through a 0.22-µm-pore-size
filter (Whatman, Inc., Ann Arbor, Mich.), acidified with 0.1 M
H2SO4, and injected (100 µl) into the HPLC.
All compounds detectable with either the UV/Vis absorbance detector or
the refractive index detector within 120 min were monitored. Volatile
fatty acids were identified by their retention times compared to those
of authentic standards on the HPX-87H column and also by gas
chromatography-flame ionization detector analysis performed with a
4-mm-inside-diameter, 183-cm-long glass column (GP10%, SP-1200/1%
H3PO4) and a Hewlett-Packard model 5890A series
II gas chromatograph. The detection limits were 34 µM for glucose, 3 µM for lactate and ethanol, 4 µM for butyrate and propionate, 5 µM for acetate, 6 µM for isobutyrate, 2 µM for succinate, and 0.2 µM for formate. Headspace hydrogen was measured with a Trace
Analytical RGA3 reduction gas analyzer, and headspace methane was
analyzed by gas chromatography (Hewlett-Packard model 5890 series II).
The detection limits for hydrogen and methane were 2.7 × 10
6 and 0.01 atm, respectively. The gas production rate
in the two reactor sets was not monitored. The measures of biomass used
included optical density at 650 nm with a 1-cm light path (OD650,
1 cm), total protein content (Comassie blue protein assay of
alkaline extract), and content of volatile suspended solids
(3). OD650, 1 cm values were experimentally
related to the content of volatile suspended solids (assumed to be
biomass) by the following relationship: biomass (in milligrams per
liter) = 442 × OD650, 1 cm.
Glucose perturbation. After the HS set was operated for 5 MCRTs (80 days) and the LS set was operated for 2 MCRTs (32 days) at an average glucose loading rate of 0.34 g/liter-day, glucose perturbation was applied simultaneously to both sets by increasing the concentration of glucose in each reactor to approximately 6.8 g/liter (38 mM). The concentrated glucose stock solution used for this purpose also contained an equivalent amount of a 50:50 mixture of sodium and potassium bicarbonates in order to provide buffer for the additional organic acids expected from fermentation of glucose. Samples were collected at appropriate intervals for soluble intermediate product analysis, as well as pH, optical density, protein, H2, and CH4 analyses. For the initial 48 h after the perturbation, a rigorous sampling schedule was used to closely monitor the accumulation of intermediate products.
The time of perturbation for each set is designated time zero, and preperturbation times are referred to by negative values (days
80 to
0 for the HS set and days 32 to 0 for the LS set). The amounts of all
soluble intermediate products were normalized to the amount of added
glucose by expressing the levels of compounds in terms of the available
electron equivalents (ee) and are expressed as percentages. Hydrogen
and methane concentrations are expressed as reactor headspace
concentrations (in atmospheres).
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RESULTS AND DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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Dynamics of the referential state.
The COD removal efficiency
before the perturbation (days 80 to 0 for the HS set and days 32 to
0 for the LS set) was 93% ± 3% for both sets of reactors. For the HS
set, the remaining COD included 1.5 ± 1.3 mM acetate, 1.2 ± 1.5 mM propionate, and 0.12 ± 0.23 mM butyrate. For the LS set,
the remaining COD included 0.89 ± 1.2 mM acetate, 0.39 ± 0.42 mM propionate, and 0.05 ± 0.13 mM butyrate. The steady-state
glucose concentrations in both reactor sets under these conditions were
below the detection limit (less than 34 µM). The headspace methane
and hydrogen concentrations in both sets were 0.50 ± 0.04 and
9 × 105 ± 0.51 × 105 atm,
respectively, and the pH of the reactor liquid was 6.91 ± 0.09. No lactate, ethanol, or any other soluble product was detected during
this period in both reactor sets by the analytical techniques used,
indicating efficient methanogenic conversion of glucose. At the time of
perturbation, the concentrations of the intermediate soluble products
in all reactors were below 1 mM each for acetate, butyrate, and
propionate. The maximum substrate utilization rate determined only for
the HS set over this period was 11.8 ± 5.5 µmol/mg of protein/h
for glucose, 4.6 ± 3.0 µmol/mg of protein/h for lactate,
1.6 ± 0.65 µmol/mg of protein/h for acetate, and 0.32 ± 0.43 µmol/mg of protein/h for butyrate. For hydrogen, this rate was
measured by monitoring methane production and was found be 7.0 ± 1.2 µmol/mg of protein/h. This indicates that there was a somewhat
lower range of activities compared to the mother reactor activities.
The biomass concentration prior to the perturbation was 428 ± 14 mg/liter in the HS set and 410 ± 27 mg/liter in the LS set, and
there was no significant difference between the two sets (P = 0.372). Hence, the stability analysis results are presented
without normalization.
Resistance, resilience, and stability.
The utilization of
glucose and the accumulation of major soluble products in response to
the perturbation are shown in Fig. 2.
Various functional stability parameters were computed by analyzing the
amplification envelope for glucose and the four dominant intermediate soluble products: lactate, butyrate, acetate, and propionate. Formate
and isobutyrate accumulated to less than 8% each and were consumed
within 2 days; therefore, these compounds were not included in the
stability analysis. No other soluble intermediate products were
observed by the analytical techniques used. Total COD analysis conducted on a subset of the reactor samples indicated that the soluble
products measured constituted most of the COD. Reactor 5 of the HS set
and reactor 4 of the LS set had anomalous performance either under
referential state or perturbed state conditions compared to the other
three reactors in the corresponding sets. This is apparent from the
accumulation of lactate, butyrate, and especially acetate in reactor 4 (Fig. 2b, c, and d) and from the accumulation of propionate in reactor
5 (Fig. 2e). The startup of reactor 5 was also poor (data not shown).
Hence, reactors 4 and 5 are excluded from the stability analysis.
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, reactor 5; 
, reactor 6; 
, reactor 7;
, reactor 8; 
, reactor 1; 
, reactor 2; 
, reactor 3; 
,
reactor 4.
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Parallel versus serial substrate processing and functional
stability.
The sequence of accumulation of the four major soluble
intermediate products in response to the glucose perturbation is shown in Fig. 3 (average of three reactors from
each set). In the HS set, the accumulations of the four intermediate
products were simultaneous in response to the glucose perturbation,
indicating a predominantly parallel flow of substrate (Fig. 3a). In the
LS set, the depletion of glucose (occurring within 20 h [Fig.
2]) coincided with the rapid accumulation of lactate, which was then converted predominantly to butyrate within 2 days (Fig. 3b). The utilization of butyrate occurred over the next 10 days, and there was
significantly greater accumulation of acetate than that in the HS set.
Accumulation of the intermediate products in the LS set was
predominantly serial (Fig. 3b).
|
G0', kJ/molLactate + 0.4 Acetate + 0.7 H+ 
0.7 Butyrate + 183.9
0.6 H2+ CO2 + 0.4 H2O Lactate + Acetate + H+ Butyrate + 0.8 H2 + 59.4 1.4
CO2 + 0.6 H2O 2 Lactate + H+ Butyrate + 2 H2 + 2 CO2 64.1
A number of organisms, including Clostridium
tyrobutyricum, Clostridium acetobutylicum, and
Butyribacterium methylotrophicum, have been
implicated in the above reactions (2, 8, 14). Since
the mother reactor for the LS set was started at a different time of
the year than the mother reactor for the HS set was started, it is
possible that it contained significantly larger populations of
organisms that can produce lactate and convert lactate to butyrate.
Replication of function under perturbed states.
As evident
from the data in Table 1 and Fig. 2, replication of the substrate flow
pattern under perturbed conditions by mixed microbial communities is
possible. It should be noted, however, that one reactor from each set
of four reactors was not included in the analysis. This could be
considered the limit to replication of complex microbial systems.
Moreover, even for the three reactors in each set, exact replication
for all intermediate products was never observed, indicating that there
is a need to define a "degree of replication." We combined the
replication in all the stability parameters using the following
equation:
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6% after 17.5 MCRTs. For these conditions, a minor
population representing 1% of an inoculum consisting of
109 cells/ml is initially present at a concentration of
107 cells/ml. After 5.8 MCRTs, 6 × 105
cells/ml are still present even with no net growth. Since such a small
population can exist in a microbial system and perhaps even find a
niche and grow, the significant deviations observed within a set in
response to the perturbation are not surprising. This also emphasizes
the point that operating a mixed-community reactor for 3 MCRTs may be
sufficient to achieve stable performance under referential state
conditions but it is evidently inadequate to achieve a high degree of
replication of stability of function under perturbed conditions.
This study supports the hypothesis that parallel processing of
substrate may confer greater functional stability in response to a
substrate perturbation. In this context, parallel should not be taken
as absolutely parallel as in some fields, but as a network of multiple
routes for substrate flow. The results also indicated that ecological
functions of similar microbial communities are replicable within the
uncertainties associated with complex systems. However, under perturbed
conditions significant deviations are possible and are most likely due
to the presence of numerically minor but important populations, as
shown in the companion paper (4). These deviations can have
a profound impact on the functional stability of such systems during perturbations.
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ACKNOWLEDGMENTS |
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This research was supported by NSF grant DEB 9120006 to the Center for Microbial Ecology. A.S.F. was partially supported by an OAS grant and by the Comisión Secretorial de Investigación Cientifica, Universidad de República, Montevideo, Uruguay.
We are grateful to Kay Gross (Kellogg Biological Station, Michigan State University) and Lugarde Raskin (University of Illinois at Urbana-Champaign) for their valuable discussions about ecological concepts throughout the course of this work.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Civil and Environmental Engineering, Michigan State University, A-126 Engineering Research Complex, E. Lansing, MI 48824. Phone: (517) 355-8241. Fax: (517) 355-0250. E-mail: hashsham{at}egr.msu.edu.
Present address: Cátedra de Microbiología, Facultad
de Química, Montevideo, Uruguay.
Present address: Department of Civil and Environmental
Engineering, Stanford University, Stanford, CA 94305.
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Abstract
Introduction
Materials and Methods
Results and Discussion
References
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Applied and Environmental Microbiology, September 2000, p. 4050-4057, Vol. 66, No. 9
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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