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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

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2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2020, Vol. 14 Issue (1) : 3    https://doi.org/10.1007/s11783-019-1182-8
RESEARCH ARTICLE
Long-term adaptive evolution of Shewanella oneidensis MR-1 for establishment of high concentration Cr(VI) tolerance
Yong Xiao1,2(), Changye Xiao1,2, Feng Zhao1,2()
1. CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China
2. University of Chinese Academy of Sciences, Beijing 100049, China
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Abstract

Shewanella oneidensis MR-1 was acclimated to grow with Cr(VI) of 190 mg/L.

• Whole genomes from 7 populations at different acclimation stages were sequenced.

• Gene mutations mainly related to efflux pumps and transporters.

• An adaptation mechanism of MR-1 to high concentration of Cr(VI) was proposed.

Acclimation is the main method to enhance the productivity of microorganisms in environmental biotechnology, but it remains uncertain how microorganisms acquire resistance to high concentrations of pollutants during long-term acclimation. Shewanella oneidensis MR-1 was acclimated for 120 days with increasing hexavalent chromium (Cr(VI)) concentrations from 10 to 190 mg/L. The bacterium was able to survive from the highly toxic Cr(VI) environment due to its enhanced capability to reduce Cr(VI) and the increased cell membrane surface. We sequenced 19 complete genomes from 7 populations of MR-1, including the ancestral strain, the evolved strains in Cr(VI) environment on days 40, 80 and 120 and their corresponding controls. A total of 27, 49 and 90 single nucleotide polymorphisms were found in the Cr(VI)-evolved populations on days 40, 80 and 120, respectively. Nonsynonymous substitutions were clustered according to gene functions, and the gene mutations related to integral components of the membrane, including efflux pumps and transporters, were the key determinants of chromate resistance. In addition, MR-1 strengthened the detoxification of Cr(VI) through gene variations involved in adenosine triphosphate binding, electron carrier activity, signal transduction and DNA repair. Our results provide an in-depth analysis of how Cr(VI) resistance of S. oneidensis MR-1 is improved by acclimation, as well as a genetic understanding of the impact of long-term exposure of microorganisms to pollution.

Keywords Environmental biotechnology      Acclimation      Chromate resistance      Efflux pumps      Detoxification     
Corresponding Author(s): Yong Xiao,Feng Zhao   
Issue Date: 30 October 2019
 Cite this article:   
Yong Xiao,Changye Xiao,Feng Zhao. Long-term adaptive evolution of Shewanella oneidensis MR-1 for establishment of high concentration Cr(VI) tolerance[J]. Front. Environ. Sci. Eng., 2020, 14(1): 3.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1182-8
https://academic.hep.com.cn/fese/EN/Y2020/V14/I1/3
Fig.1  Growth rate (black line) and reduction kinetics (red line) of ancestral and evolved S. oneidensis MR-1 strains in different initial concentrations of hexavalent chromium Cr(VI). (A) The growth curves of ancestral strain D0 cultured in Luria-Bertani (LB) broth without Cr(VI) and with 90mg/L Cr(VI) (inset). (B) Evolved strain at day 40 (population D40Cr) was inoculated in LB broth with 90 mg/L Cr(VI). (C) Evolved strain at day 80 (population D80Cr) was inoculated in LB broth with 140 mg/L Cr(VI). (D) Evolved strain at day 120 (population D120Cr) was inoculated to LB broth with 190 mg/L Cr(VI).
Fig.2  Number of SNP mutations in 6 evolved populations. Populations D40, D80 and D120 were strains derived from ancestral MR-1 and cultured in LB medium without chromium for 40, 80 and 120 days, respectively. Populations D40Cr, D80Cr and D120Cr were evolved MR-1 strains cultured for 40, 80 and 120 days in LB broth with increasing levels of hexavalent chromium. Each population has three replicates, and the red, green and blue bars represent group A, B and C in each population, respectively.
Fig.3  Most enriched Gene Ontology (GO) terms of mutated genes in population D120Cr. The P-value from the result of enrichment analysis was the X-axes and Y-axes was the GO terms in DAVID functional analysis, which included three categories, namely, biological process, cellular component and molecular function.
Fig.4  (a) Distribution of nonsynonymous substitutions across the whole genome between different evolved mutants. Rings from outermost to innermost represent the population D120Cr, D80Cr, D40Cr and ancestral D0, and all genes with nonsynonymous mutations are labeled in coding regions. The orange and aqua dots represent stop-gain mutations and the same mutations that occurred in the evolved populations, respectively. (b) Number of non-synonymous substitution in the 6 evolved populations. Each population has three replicates. The red, green and blue bars represent isolates A, B and C, respectively.
Fig.5  Functional groups of the missense mutations among populations D40Cr, D80Cr and D120Cr which were inoculated in Cr(VI)-containing medium for 40, 80 and 120 days. Displayed are the different functional categories of the missense mutated genes that use KEGG and GO terms performed with DAVID v.6.8. The percentage value corresponds to the number of missense mutated genes in each functional category.
Fig.6  Missense mutated genes across integral component of the membrane in Shewanella oneidensis MR-1. (A) Sulfate uptake channel which is also used by chromate. (B) Efflux pump component of membrane. (C) Transporter encoded by genes which transport substances to ensure the metabolic function. (D) Signal transducer activities. (E) Electron carrier enzyme to take part in the reduction of Cr(VI). (F) DNA binding.
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