Anaerobic Demethylation
During his Diplom and PhD thesis with Bernhard Schink, Jan worked with a novel homoacetogenic bacterium because of its unusual features. It was named it Holophaga foetida since it completely (holos) eats (phagein) its aromatic substrates (both the phenolic ring and the methyl groups of phenyl methyl ethers) and stinks (foetidus) due to the production of dimethyl sulfide from the methyl groups of the phenyl methyl ethers.
Sketch of the branched catabolism of methylated phenolic plant compounds by Holophaga foetida. Four pathways are involved in the degradation of phenyl methyl ethers: (1) demethylation, (2) aromatic ring degradation by the phloroglucinol pathway,(3) sulphide methylation, and (4) methyl carbonylation by the acetyl-CoA pathway.
Holophaga foetida is a fascinating bacterium that among other things combines the two pathways of demethylation and ring degradation, that were known from its competitors, into one longer pathway, which yields more ATP, but the bacteria grow more slowly than the competitors that only demethylate or only degrade the aromatic ring. Nevertheless, Holophaga foetida is numerically more abundant than the faster growing competitors in all the sediments that we tested. During work in the Schink Lab Jan did not understand why this bacterium grew more slowly, but many years later while at Bonn, came across this kinetic theory that can in fact explain this observation.
Survival of the shortest pathway: why is metabolic labour divided in nitrification?
Kinetic theory of optimal pathway length can explain the metabolic division of labour between ammonia-oxidizing and nitrite-oxidizing bacteria.
Winogradsky discovered in 1890 that nitrification, the process of oxidizing ammonia to nitrate, is carried out in two consecutive steps by two physiologically and phylogenetically distinct groups of bacteria: ammonia oxidizing bacteria and nitrite oxidising bacteria.
Step 1: ammonia oxidation to nitrite (AOB: Ammonia Oxidizing Bacteria)
NH4+ + 1.5 O2 → 2 H+ + NO2- + H2O
ΔGº' = -275 kJ/mol N or -46 kJ/mol e-, Eº' = 343 mV
Step 2: nitrite oxidation to nitrate (NOB: Nitrite Oxidizing Bacteria)
NO2- + 0.5 O2 → NO3-
ΔGº' = -74 kJ/mol N or -37 kJ/mol e-, Eº' = 434 mV
To date, no exceptions to this rule are known, but the reasons for this division of labour have not received much attention. We offer an explanation for this cross-feeding based on kinetic theory of optimal pathway design, which assumes that the production of enzymes as well as the presence of intermediates is costly and that the number of ATP generating steps is proportional to the length of the pathway. From these assumptions, the existence of an optimal pathway length follows which maximises the rate of ATP production. Shortening the pathway could therefore increase the rate of ATP production and growth, increasing fitness in environments such as enrichment cultures that select for fastest growth rate. However, there is a trade-off between growth rate and growth yield, since the longer pathway would have more ATP generating steps, thereby increasing growth yield, which has been shown to be advantageous when bacteria grow in clonal clusters, as is typical for biofilms (See the project on Biofilms promote altruism). We postulate the existence of bacteria that completely oxidize ammonia to nitrate. Isolation of these "lithotrophs missing in nature" requires selection for higher yield, for which biofilm but not batch enrichments might be used.
For more information, please consult our paper:
Costa E, Pérez J, Kreft JU (2006) Why is metabolic labour divided in nitrification? Trends in Microbiology 14, 213-219
Key references
- Bock E, Wagner M (2001) Oxidation of inorganic nitrogen compounds as an energy source. In: The Prokaryotes: An evolving electronic resource for the microbiological community, 3rd edition, release 3.7, Dworkin M (ed), New York: Springer-Verlag
- Broda E (1977) Two kinds of lithotrophs missing in nature. Z Allg Mikrobiol 17, 123-143
- Kreft JU (2004) Biofilms promote altruism. Microbiology 150, 2751-2760
- Kreft JU, Bonhoeffer S (2005) The evolution of groups of cooperating bacteria and the growth rate versus yield trade-off. Microbiology 151, 637-641
- Pfeiffer T, Bonhoeffer S (2004) Evolution of cross-feeding in microbial populations. Am Nat 163, E126-E135
- Pfeiffer T, Schuster S, Bonhoeffer S (2001) Cooperation and competition in the evolution of ATP-producing pathways. Science 292, 504-507