Cultivation of Aquincola tertiaricarbonis L108 on the fuel oxygenate intermediate tert-butyl alcohol induces aerobic anoxygenic photosynthesis at extremely low feeding rates

Abstract

Aerobic anoxygenic photosynthesis (AAP) is found in an increasing number of proteobacterial strains thriving in ecosystems ranging from extremely oligotrophic to eutrophic. Here, we have investigated whether the fuel oxygenate-degrading betaproteobacterium Aquincola tertiaricarbonis L108 can use AAP to compensate kinetic limitations at low heterotrophic substrate fluxes. In a fermenter experiment with complete biomass retention and also during chemostat cultivation, strain L108 was challenged with extremely low substrate feeding rates of tert-butyl alcohol (TBA), an intermediate of methyl tert-butyl ether (MTBE). Interestingly, formation of photosynthetic pigments, identified as bacteriochlorophyll a and spirilloxanthin, was only induced in growing cells at TBA feeding rates less than or equal to maintenance requirements observed under energy excess conditions. Growth continued at rates between 0.001 and 0.002 h "1 even when the TBA feed was decreased to values close to 30 % of this maintenance rate. Partial sequencing of genomic DNA of strain L108 revealed a bacteriochlorophyll synthesis gene cluster (bchFNBHL) and photosynthesis regulator genes (ppsR and ppaA) typically found in AAP and other photosynthetic proteobacteria. The usage of light as auxiliary energy source enabling evolution of efficient degradation pathways for kinetically limited heterotrophic substrates and for lowering the threshold substrate concentration S min at which growth becomes zero is discussed.

RpoN (σ 54 ) Is Required for Floc Formation but Not for Extracellular Polysaccharide Biosynthesis in a Floc-Forming Aquincola tertiaricarbonis Strain

“…S2A) (10). The draft genome sequencing assembly and annotation revealed that the RN12 strain harbored the previously characterized gene clusters for biosynthesis of bacteriochlorophyll (bch) and anoxygenic photosynthesis, as well as the gene for leucine/isovalerate utilization (liu), encoded in the A. tertiaricarbonis strain L108 (3,11). The average nucleotide identity (ANI) of the common genes between L108 and RN12 was also relatively high.…”

Fixation of CO2 using the ethylmalonyl‐CoA pathway in the photoheterotrophic marine bacterium Dinoroseobacter shibae

“…Bacteriochlorophyll synthesis has been shown to be induced under carbon limitation (Sato-Takabe et al, 2014) or under osmotic stress (Biebl, 2006), and light prolonged survival of the Roseobacter species Dinoroseobacter shibae under starvation (Soora and Cypionka, 2013;Soora et al, 2015). During biodegradation of tertyl-butyl alcohols in a chemostat, bacteriochlorophyll synthesis was unexpectedly induced at extremely low substrate concentrations; the photosynthesis gene cluster was subsequently detected in the genome of the strain (Rohwerder et al, 2013). The first metabolic model of an AAP taking into account the role of light as an additional source of energy demonstrated a direct effect of light on swimming speed of D. shibae (Rex et al, 2013).…”

Phylogenetically Diverse Aerobic Anoxygenic Phototrophic Bacteria Isolated from Epilithic Biofilms in Tama River, Japan

“…2 ). Only two species, Roseateles depolymerans ( 42 ) and Aquincola tertiaricarbonis ( 27 , 35 ) have been described as AAP bacteria in Betaproteobacteria . Other aerobic Betaproteobacteria such as Methyloversatilis unversalis and Limnohabitans sp.…”

“…Elioraea tepidiphila , which has been described as a non-phototrophic bacterium, was shown to have pufLM gene sequences in its genome ( 1 ). A. tertiaricarbonis was also initially described as a non-phototrophic bacterium that does not produce BChl, but was subsequently found to produce BChl under different culture conditions ( 27 , 35 ). These examples suggest that some bacteria described as non-phototrophic may have photosynthesis genes and produce a photosynthetic apparatus under some conditions.…”