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(Per)Chlorate-Reducing Bacteria Can Utilize Aerobic and Anaerobic Pathways of Aromatic Degradation with (Per)Chlorate as an Electron Acceptor

机译:减少(氯酸盐)的细菌可以利用(氯)酸盐作为电子受体的好氧和厌氧途径进行芳香分解。

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ABSTRACT The pathways involved in aromatic compound oxidation under perchlorate and chlorate [collectively known as (per)chlorate]-reducing conditions are poorly understood. Previous studies suggest that these are oxygenase-dependent pathways involving O_(2)biogenically produced during (per)chlorate respiration. Recently, we described Sedimenticola selenatireducens CUZ and Dechloromarinus chlorophilus NSS, which oxidized phenylacetate and benzoate, two key intermediates in aromatic compound catabolism, coupled to the reduction of perchlorate or chlorate, respectively, and nitrate. While strain CUZ also oxidized benzoate and phenylacetate with oxygen as an electron acceptor, strain NSS oxidized only the latter, even at a very low oxygen concentration (1%, vol/vol). Strains CUZ and NSS contain similar genes for both the anaerobic and aerobic-hybrid pathways of benzoate and phenylacetate degradation; however, the key genes ( paaABCD ) encoding the epoxidase of the aerobic-hybrid phenylacetate pathway were not found in either genome. By using transcriptomics and proteomics, as well as by monitoring metabolic intermediates, we investigated the utilization of the anaerobic and aerobic-hybrid pathways on different electron acceptors. For strain CUZ, the results indicated utilization of the anaerobic pathways with perchlorate and nitrate as electron acceptors and of the aerobic-hybrid pathways in the presence of oxygen. In contrast, proteomic results suggest that strain NSS may use a combination of the anaerobic and aerobic-hybrid pathways when growing on phenylacetate with chlorate. Though microbial (per)chlorate reduction produces molecular oxygen through the dismutation of chlorite (ClO_(2)~(?)), this study demonstrates that anaerobic pathways for the degradation of aromatics can still be utilized by these novel organisms. IMPORTANCE S.?selenatireducens CUZ and D.?chlorophilus NSS are (per)chlorate- and chlorate-reducing bacteria, respectively, whose genomes encode both anaerobic and aerobic-hybrid pathways for the degradation of phenylacetate and benzoate. Previous studies have shown that (per)chlorate-reducing bacteria and chlorate-reducing bacteria (CRB) can use aerobic pathways to oxidize aromatic compounds in otherwise anoxic environments by capturing the oxygen produced from chlorite dismutation. In contrast, we demonstrate that S.?selenatireducens CUZ is the first perchlorate reducer known to utilize anaerobic aromatic degradation pathways with perchlorate as an electron acceptor and that it does so in preference over the aerobic-hybrid pathways, regardless of any oxygen produced from chlorite dismutation. D.?chlorophilus NSS, on the other hand, may be carrying out anaerobic and aerobic-hybrid processes simultaneously. Concurrent use of anaerobic and aerobic pathways has not been previously reported for other CRB or any microorganisms that encode similar pathways of phenylacetate or benzoate degradation and may be advantageous in low-oxygen environments.
机译:摘要在高氯酸盐和氯酸盐(统称为(全)氯酸盐)还原条件下参与芳族化合物氧化的途径知之甚少。先前的研究表明,这些是氧合酶依赖性途径,涉及在(全)氯酸盐呼吸过程中生物产生的O_(2)。最近,我们描述了Sedimenticola selenatireducens CUZ和Dechloromarinus philphilus NSS,它们氧化苯乙酸盐和苯甲酸盐(芳香族化合物分解代谢中的两个关键中间体),分别还原高氯酸盐或氯酸盐和硝酸盐。尽管菌株CUZ还用氧气作为电子受体氧化了苯甲酸酯和苯乙酸盐,但即使在非常低的氧气浓度(1%,体积/体积)下,菌株NSS也会仅氧化后者。菌株CUZ和NSS的苯甲酸和乙酸苯酯降解的厌氧和好氧混合途径均含有相似的基因。然而,在任何一个基因组中都没有发现编码有氧-混合苯乙酸途径的环氧化酶的关键基因(paaABCD)。通过使用转录组学和蛋白质组学,以及通过监测代谢中间体,我们研究了厌氧和好氧混合途径在不同电子受体上的利用。对于菌株CUZ,结果表明利用了以高氯酸盐和硝酸盐为电子受体的厌氧途径,以及在有氧条件下利用了好氧-混合途径。相反,蛋白质组学结果表明,当NSS菌株在含氯乙酸的苯乙酸酯上生长时,可能会结合使用厌氧和好氧混合途径。尽管微生物(全)氯酸盐的还原通过亚氯酸盐(ClO_(2)〜(?))的分解而产生了分子氧,但这项研究表明,这些新型生物仍然可以利用厌氧途径降解芳烃。重要提示S.?enenatereducensens CUZ和D.?philphilus NSS分别是(过)氯酸盐和氯酸盐减少细菌,它们的基因组均编码厌氧和好氧混合途径,以降解苯乙酸和苯甲酸。以前的研究表明,减少(过)氯酸盐的细菌和减少氯酸盐的细菌(CRB)可以利用有氧途径,通过捕获亚氯酸盐歧化产生的氧气,在其他缺氧环境中氧化芳香化合物。相比之下,我们证明了硒化链霉菌CUZ是已知的第一个利用高氯酸盐作为电子受体利用厌氧芳香族降解途径的高氯酸盐还原剂,并且无论亚氯酸盐产生的任何氧气如何,它都比有氧-杂交途径优先使用变异。另一方面,嗜盐链球菌NSS可能同时进行厌氧和好氧混合过程。对于其他CRB或任何编码相似的乙酸苯酯或苯甲酸酯降解途径的微生物,以前尚未见到厌氧和好氧途径同时使用的报道,并且在低氧环境中可能是有利的。

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