Benzoate mediates the simultaneous repression of anaerobic 4-methylbenzoate and succinate utilization in Magnetospirillum sp. strain pMbN1

BMC Microbiology

Ralf Rabus¹  Lars Wöhlbrand²  Marvin Dörries²  Annemieke Strijkstra¹  Kathleen Trautwein¹  Sven Lahme¹ 

[1] Max Planck Institute for Marine Microbiology, Bremen, Germany;Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University Oldenburg, Oldenburg, Germany

关键词: Proteomics;    Transcript analysis;    Physiology;    Ternary substrate mixture;    Diauxie;    Repression;    Aromatic compounds;    4-Methylbenzoate;    Anaerobic degradation;   

Others  :  1137741
DOI  :  10.1186/s12866-014-0269-4

 received in 2014-07-30, accepted in 2014-10-15,  发布年份 2014

【 摘 要 】

Background

At high concentrations of organic substrates, microbial utilization of preferred substrates (i.e., supporting fast growth) often results in diauxic growth with hierarchical substrate depletion. Unlike the carbon catabolite repression-mediated discriminative utilization of carbohydrates, the substrate preferences of non-carbohydrate-utilizing bacteria for environmentally relevant compound classes (e.g., aliphatic or aromatic acids) are rarely investigated. The denitrifying alphaproteobacterium Magnetospirillum sp. strain pMbN1 anaerobically degrades a wide variety of aliphatic and aromatic compounds and is unique for anaerobic degradation of 4-methylbenzoate. The latter proceeds via a distinct reaction sequence analogous to the central anaerobic benzoyl-CoA pathway to intermediates of central metabolism. Considering the presence of these two different anaerobic “aromatic ring degrading” pathways, substrate preferences of Magnetospirillum sp. strain pMbN1 were investigated. Anaerobic growth and substrate consumption were monitored in binary and ternary mixtures of 4-methylbenzoate, benzoate and succinate, in conjuction with time-resolved abundance profiling of selected transcripts and/or proteins related to substrate uptake and catabolism.

Results

Diauxic growth with benzoate preference was observed for binary and ternary substrate mixtures containing 4-methylbenzoate and succinate (despite adaptation of Magnetospirillum sp. strain pMbN1 to one of the latter two substrates). On the contrary, 4-methylbenzoate and succinate were utilized simultaneously from a binary mixture, as well as after benzoate depletion from the ternary mixture. Apparently, simultaneous repression of 4-methylbenzoate and succinate utilization from the ternary substrate mixture resulted from (i) inhibition of 4-methylbenzoate uptake, and (ii) combined inhibition of succinate uptake (via the two transporters DctPQM and DctA) and succinate conversion to acetyl-CoA (via pyruvate dehydrogenase). The benzoate-mediated repression of C₄-dicarboxylate utilization in Magnetospirillum sp. strain pMbN1 differs from that recently described for “Aromatoleum aromaticum” EbN1 (involving only DctPQM).

Conclusions

The preferential or simultaneous utilization of benzoate and other aromatic acids from mixtures with aliphatic acids may represent a more common nutritional behavior among (anaerobic) degradation specialist than previously thought. Preference of Magnetospirillum sp. strain pMbN1 for benzoate from mixtures with 4-methylbenzoate, and thus temporal separation of the benzoyl-CoA (first) and 4-methylbenzoyl-CoA (second) pathway, may reflect a catabolic tuning towards metabolic efficiency and the markedly broader range of aromatic substrates feeding into the central anaerobic benzoyl-CoA pathway.

【 授权许可】

   
2014 Lahme et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

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