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Diss. ETH No. 11905 the PHYSIOLOGY of a DEFINED Diss. ETH No. 11905 THE PHYSIOLOGY OF A DEFINED FOUR-MEMBERED MIXED BACTERIAL CULTURE DURING CONTINUOUS CULTIVATION WITH MIXTURES OF THREE POLLUTANTS IN SYNTHETIC SEWAGE A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH for the degree of Doctor of Natural Sciences Presented by ALBERT JUNG TIEN M.S. (Life Sciences) New Mexico Highlands University, USA born 1 August, 1965 citizen of the United States of America accepted on the recommendation of Prof. Dr. Th. Leisinger, examiner Prof. Dr. P. Peringer, co-examiner PD. Dr. Th. Egli, co-examiner TABLE OF CONTENTS Summary ................, ............................................... 1 Zusammenfassung •...•....••.....•.•••.•.•..••.•..................••.• 4 1 . Introduction ............................................................ 8 2 . Regulation of pollutant degradation in the presence of an alternative substrate by the para-toluenesulfonate utilizing Comamonas testosteroni strain T-2 and the dichloromethane utilizing Methylobacterium strain DM4 during growth in batch and continuous culture ..••••. 31 3. Growth of Methylobacterium strain DM4 in continuous culture: Effects of dilution rate and response to substrate shifts during continuous cultivation .............................................................. 5 8 4. Dynamics of substrate consumption and enzyme activity by Comamonas testosteroni strain T-2 in response to carbon substrate shifts in carbon-limited continuous cultures ..........•.....•..........•....•.........••...•..• 82 5 . Dynamics and regulation of mixed pollutant degradation by a four-membered defined bacterial consortium in continuous culture•.•.•...•..•.......•••.•....•...• 101 6. Conclusions ............................................................. 126 7. Appendix 1) Combined ozonation and biological treatment for the removal of a model refractory compound, toluenesulfonate, from simulated industrial wastewater ....... 139 2) Microbially mediated formation of struvite by Methylobacterium strain DM4: Biotechnological applications ............................................................. 1' ••••••• 143 3) Microbial mediation as a possible mechanism for natural dolomite formation at low temperature ................... 16 6 I Summary SUMMARY The influence of mixed substrate utiHzation on the growth and survival of three pollutant utilizing microorganisms: Comamonas testosteroni strain T-2, a toluenesulfonate (TS) degrader; Methylobacterium strain DM4, a dichloromethane (DCM) degrader; Chelatobacter heintzii strain 29600, a nitrilotriacetate (NT A) degrader; and the non-pollutant degrading Escherichia coli strain ML30; was investigated using pure cultures and a defined mixed culture composed of the four bacterial strains under both batch and continuous cultivation conditions. The purpose of these investigations was to determine the following: 1) Does the presence of easily utilizable substrates inhibit the utilization of a pollutant as a carbon/energy source? 2) Do common trel1lds exist concerning mixed substrate utilization (pollutant and easily utilizable carbon substrates) in evolutionarily distinct microbial species which utilize structurally different chemical pollutants? 3) Does the ability to simultaneously utilize pollutant and easily utilizable substrates give these organisms a competitive advantage over other microorganisms found. in the environment? 4) Can patterns of regulation, especially with respect to the degradation of pollutants in the presence of other easily utilizable substrates be extrapolated to more complex systems; i.e. Is what we observe in pure culture (mixed substrate/pollutant utilization) also seen in nature? In batch culture, C. testosteroni strain T-2 utilized acetate and TS simultaneously. For Methylobacterium strain DM4, substrate utilization patterns were highly dependent on precultivation conditions. Whereas DCM pregrown cultures of Methylobacterium strain DM4 were able to simultaneously utilize acetate and DCM, acetate precultivated cultures of strain DM4 exhibited diauxic growth with acetate utilized first. 2 Summary Simultaneous utilization of both pollutant and altemati ve substrate was always demonstrated during carbon-limited growth in continuous cultures. In both strains induction of the pollutant degrading systems occurred when the pollutant contributed to approximately 1% of the total carbon supplied in the feed. Maximal induction levels were achieved when the pollutant contributed to approximately 3% in the case of C. testosteroni strain T-2, and 5% in the case of Methylobacterium strain DM4. When steady-state cultures (D=0.05 hr-1) experienced shifts from acetate to DCM in the feed, a two stage induction pattern was observed (as demonstrated by excess substrate specific oxygen uptake measurements) with approximately 30 hrs elapsing before maximal induction was acheived (twenty fold over constitutive level). Levels of DCM dehalogenase protein (quantified by Western blotting) paralleled excess substrate specific oxygen uptake rates. A similar induction pattern as that seen during a transient from acetate to DCM was observed when Methylobacterium strain DM4 cultivated with synthetic sewage, was shifted to a medium consisting of synthetic sewage containing 10% DCM. In a continuous culture of C. testosteroni strain T-2, replacing acetate with TS in the feed, a sigmoidal induction pattern in pollutant degrading activity was seen. Similar induction patterns were observed when acetate was replaced with 10% TS/90% acetate and also 40% TS/60% acetate. As with the case of Methylobacterium strain DM4, simultaneous utilization of alternative substrates by C. testosteroni strain T-2 increased the rate of new enzyme synthesis. During batch growth with the four strains in a synthetic sewage containing the specific pollutants, E. coli strain ML30 outnumbered its nearest competitor, C. testosteroni strain T-2, approximately 2:1. Methylobacterium strain DM4 and C. heintzii strain 29600 were present 3 Summary at approximately half the levels as C. testosteroni strain T-2. In continuous culture (D=0.05 hr-1) coexistance of the four strains was achieved (55%£. coli strain ML30, 15% C. testosteroni strain T-2, 15% Methylobacterium strain DM4 and 15% C. heintzii strain 29600 ). When NTA, TS or DCM was omitted from the feed, total cell counts were only slightly lower and no significant changes in the ratio of individual str,ains were measured. When NT A, TS or DCM was replaced in the feed, induction of the specific pollutant degrading system, as monitored by increased excess substrate specific oxygen uptake rates, were observed after a lag period. No enrichment in the population of the specific pollutant degrading strain was observed. The stability of our model system can be attributed to the ability of the pollutant degrading strains to utilize not only their specific pollutants but also synthetic sewage (mixed substrate utilization) under the carbon-limited conditions imposed on the four microorganisms. Data indicate that in our case, induction of the necessary enzyme systems and not enrichment of the pollutant degrading strains is the primary mechanism that leads to pollutant removal, especially when the ratio of pollutant to available carbon is low. -----·-------------r------r---· 4 Zusammenfassung ZUSAMMENFASSUNG Der Einfluss der Verwertung von Gemischen von Kohlenstoffsubstraten auf das Wachtum und Uberleben der drei schadstoffabbauenden Mikroorganismen [Coma.monas testosteroni Stamm T-2, p-Toluolsufonat (TS) abbauendes Bakterium; Methylobacterium Stamm DM4, baut Dichlormethan (DCM) ab; Chelatobacter heintzii Stamm 29600, verwertet Nitrilotriacetat (NTA)] und Escherichia coli Stamm ML30 (vermag keinen der drei Schadstoffe abzubauen) wurde in Batch und kontinuierlicher Kultur sowohl an Reinkulturen, als auch in definierten · Mischkulturen untersucht. Das Ziel dieser Untersuchungen war es, die folgenden Fragen zu beantworten: 1) Hemmt oder verhindert die Anwesenheit leicht verwertbarer Kohlenstoffsubstrate den Abbau der Schadstoffe? 2) Gibt es fiir entfernt verwandte Bakterienstiimrne gememsame (generelle) Verhaltensmuster fiir den Abbau von Mischsubstraten (bier leicht verwertbare Kohlenstoffquellen gemeinsam mit den drei strukturell sehr unterschiedlichen Schadstoffen)? 3) Verleiht die Fahigkeit Gemische von Kohlenstoffquellen gleichzeitig zu verwerten (Mischsubstratwachstum) einem Bakterium in der Umwelt gegeniiber anderen Bakterienstammen einen Vorteil im Wettbewerb um Nahrung? 4) Konnen Verhaltensmuster beziiglich der gleichzeitigen Verwertung von leicht abbaubaren Kohlenstoffquellen und Schadstoffen, welche in Reinkulturen im Labor beobachtet werden, auf die komplexen Umwelt- oder Klaranlagenbedingungen iibertragen werden? 5 Zusammenfassung Reinkulturen von C. testosteroni Stamm T-2 verwerteten Acetat und TS in Batchkultur immer simultan. Filr Methylobacterium Stamm DM4 war das Verwertungsmuster von den Vorkulturbedingungen abhangig: Wahrend DCM vorgewachsene Zellen Acetat und DCM gleichzeitig verwerteten, zeigten Acetat vorgewachsene Kulturen eine klare Diauxie mit Praferenz fiir Acetat. In kohlenstofflimitierter kontinuierlicher Kultur (D=0.05 hr-1) verwerteten beide Stamme Acetat zusammen mit TS, respektive DCM, unabhangig vom angebotenen Mischungsverhfiltnis der beiden Kohlenstoffquellen. Bei beiden Stammen wurden die am Schadstoffabbau beteiligten Enzyme deutlich induziert, wenn der Anteil des Schadstoffs am gesamten im Medium angebotenen Kohlenstoffs 1 % ilberschritt. Maximale
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