Thermal adaptation strategies of the extremophile bacterium Thermus filiformis based on multi-omics analysis
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Thermus filiformis is an aerobic thermophilic bacterium isolated from a hot spring in New Zealand. The experimental study of the mechanisms of thermal adaptation is important to unveil response strategies of the microorganism to stress. In this study, the main pathways involved on T. filiformis thermoadaptation, as well as, thermozymes with potential biotechnological applications were revealed based on omics approaches. The strategy adopted in this study disclosed that pathways related to the carbohydrate metabolism were affected in response to thermoadaptation. High temperatures triggered oxidative stress, leading to repression of genes involved in glycolysis and the tricarboxylic acid cycle. During heat stress, the glucose metabolism occurred predominantly via the pentose phosphate pathway instead of the glycolysis pathway. Other processes, such as protein degradation, stringent response, and duplication of aminoacyl-tRNA synthetases, were also related to T. filiformis thermoadaptation. The heat-shock response influenced the carotenoid profile of T. filiformis, favoring the synthesis of thermozeaxanthins and thermobiszeaxanthins, which are related to membrane stabilization at high temperatures. Furthermore, antioxidant enzymes correlated with free radical scavenging, including superoxide dismutase, catalase and peroxidase, and metabolites, such as oxaloacetate and α-ketoglutarate, were accumulated at 77 °C.
KeywordsTranscriptomics Proteomics Metabolomics Thermozeaxanthins Peroxyl radical scavenging activity
We gratefully acknowledge the provision of time at the NGS and MAS facilities (CTBE and LNBio, respectively) of the National Center for Research in Energy and Materials. This work was financially supported by grants from CNPq (442333/2014-5 and 310186/2014-5) and FAPESP (10/18198-3). FM received a fellowship from CNPq (142685/2010-0).
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Conflict of interest
The authors declare no conflict of interest.
- Benitez A, Sánchez O (2009) Evaluation of agro-industrial by-products for α-galactosidase production by aspergillus oryzae in submerged culture. In: 9th international conference on chemical and process engineering, pp 1155–1160Google Scholar
- Giavalisco P, Li Y, Matthes A et al (2011) Elemental formula annotation of polar and lipophilic metabolites using (13) C, (15) N and (34) S isotope labelling, in combination with high-resolution mass spectrometry. Plant J 68:364–376. doi: 10.1111/j.1365-313X.2011.04682.x CrossRefPubMedGoogle Scholar
- Hamid AA, Aiyelaagbe OO, Usman LA et al (2010) Antioxidants: its medicinal and pharmacological applications. Afr J Pure Appl Chemostry 4:142–151Google Scholar
- Hanna SL, Sherman NE, Kinter MT, Goldberg JB (2000) Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry. Microbiology 146:2495–2508CrossRefPubMedGoogle Scholar
- Mandelli F, Yamashita F, Pereira J, Mercadante A (2012b) Evaluation of biomass production, carotenoid level and antioxidant capacity produced by Thermus filiformis using fractional factorial design. Braz J Microbiol 43:126–134. doi: 10.1590/S1517-83822012000100014 CrossRefPubMedPubMedCentralGoogle Scholar
- Mandelli F, Ramires BO, Couger MB et al (2015) Draft genome sequence of the thermophile Thermus filiformis ATCC 43280, producer of carotenoid—(di) glucoside-branched fatty acid (di) esters and source of hyperthermostable enzymes of biotechnological interest. Genome Announc 3(3):e00475–15. doi: 10.1128/genomeA.00475-15 CrossRefPubMedPubMedCentralGoogle Scholar
- Pintea A, Bunea A, Andrei S (2013) Impact of esterification on the antioxidant capacity of β-cryptoxanthin. Bull USAMV Anim Sci Biotechnol 70:79–85Google Scholar
- Ramaley RF, Hixson J (1970) Isolation of a nonpigmented, thermophilic bacterium similar to Thermus aquaticus. J Bacteriol 103:526–528Google Scholar
- Rodrigues E, Mariutti LRB, Chisté RC, Mercadante AZ (2012a) Development of a novel micro-assay for evaluation of peroxyl radical scavenger capacity: application to carotenoids and structure–activity relationship. Food Chem 135:2103–2111. doi: 10.1016/j.foodchem.2012.06.074 CrossRefPubMedGoogle Scholar
- Sun J, Zhou J, Wang Z et al (2015) Multi-omics based changes in response to cadmium toxicity in Bacillus licheniformis A. R Soc Chem 5:7330–7339Google Scholar