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Soil Acidobacteria Strain AB23 Resistance to Oxidative Stress Through Production of Carotenoids

  • Soil Microbiology
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Abstract

Metagenomic studies revealed the prevalence of Acidobacteria in soils, but the physiological and ecological reasons for their success are not well understood. Many Acidobacteria exhibit carotenoid-related pigments, which may be involved in their tolerance of environmental stress. The aim of this work was to investigate the role of the orange pigments produced by Acidobacteria strain AB23 isolated from a savannah-like soil and to identify putative carotenoid genes in Acidobacteria genomes. Phylogenetic analysis revealed that strain AB23 belongs to the Occallatibacter genus from the class Acidobacteriia (subdivision 1). Strain AB23 produced carotenoids in the presence of light and vitamins; however, the growth rate and biomass decreased when cells were exposed to light. The presence of carotenoids resulted in tolerance to hydrogen peroxide. Comparative genomics revealed that all members of Acidobacteriia with available genomes possess the complete gene cluster for phytoene production. Some Acidobacteriia members have an additional gene cluster that may be involved in the production of colored carotenoids. Both colored and colorless carotenoids are involved in tolerance to oxidative stress. These results show that the presence of carotenoid genes is widespread among Acidobacteriia. Light and atmospheric oxygen stimulate carotenoid synthesis, but there are other natural sources of oxidative stress in soils. Tolerance to environmental oxidative stress provided by carotenoids may offer a competitive advantage for Acidobacteria in soils.

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Funding

This study was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001. Grant No. 88881.062152/2014-01

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Authors and Affiliations

  1. Graduate Program in Genomic Sciences and Biotechnology, Catholic University of Brasília, SGAN 916 Módulo B Avenida W5 - Asa Norte, Brasília, 70790-160, Brazil

    Otávio Henrique Bezerra Pinto, Flávio Silva Costa, Gisele Regina Rodrigues, Rosiane Andrade da Costa & Cristine Chaves Barreto

  2. Laboratory of Enzymology, Institute of Biological Sciences, Department of Cell Biology, University of Brasília, Brasília, 70910-900, Brazil

    Otávio Henrique Bezerra Pinto

  3. Institute of Microbiology, Friedrich Schiller University Jena, Neugasse 25, 07743, Jena, Germany

    Flávio Silva Costa

  4. Research Center René Rachou, Oswaldo Cruz Foundation (Fiocruz), Avenida Augusto de Lima 1715, Barro Preto, Belo Horizonte, 30190-002, Brazil

    Gabriel da Rocha Fernandes

  5. Department of Physiological Sciences, Institute of Biological Sciences, Universidade de Brasília, Brasília, DF, 70910-900, Brazil

    Osmindo Rodrigues Pires Júnior

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  1. Otávio Henrique Bezerra Pinto
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Figure S1

Red/orange pigments exhibited by Occallatibacter sp. AB23 under (A) Light (top) and dark (bottom) and (B) agar stab inoculation on semi-solid medium, providing an oxygen gradient with the agar surface exposed to atmospheric concentrations of oxygen (~20%). (PDF 47057 kb)

Figure S2

(A) Chromatogram of pigment extracted from Occallatibacter sp. AB23 grown under light. (B) Diode array absorbance spectra of the chromatographic fractions. RT: retention time of each fraction corresponding to the chromatogram above. (PDF 173 kb)

Figure S3

Cell viability and production of red pigment by Occallatibacter sp. AB23 in the presence or absence of vitamins and trace elements on VL-55 medium. Colonies of Occallatibacter sp. AB23 in different treatments and dilutions. Treatments: both vitamins and trace elements (V + T); vitamins without trace elements (V); trace elements without vitamins (T); and without vitamins or trace elements (NA). Cell inoculum (no dilution), dilutions of 101, 10−2, 10−3, and 10−4. The scale bar is 100 mm. (PDF 36005 kb)

Figure S4

Putative pathway of carotenoids in Acidobacteria. The names of the enzymes are hpnC, squalene synthase; ctrB, 15-cis phytoene synthase; crtI, phytoene desaturase; ctrQ, 9,9′-di-cis-zeta-carotene desaturase or 4,4′-diaponeurosporenoate glycosyltransferase, crtP, diapolycopene oxygenase; and crtO, glycosyl-4,4′-diaponeurosporenoate acyltransferase. The genes not detected were assigned to “?”. (PDF 600 kb)

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Pinto, O.H.B., Costa, F.S., Rodrigues, G.R. et al. Soil Acidobacteria Strain AB23 Resistance to Oxidative Stress Through Production of Carotenoids. Microb Ecol 81, 169–179 (2021). https://doi.org/10.1007/s00248-020-01548-z

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