Elena SF, Lenski RE. Metabolic flexibility of sulfate-reducing bacteria. We further analyzed potential effects of mutations on functions of their associated genes/proteins in the six functional groups. For the other 27 mutated genes with 35 newly acquired mutations, we found seven genes with 17 new mutations acquired in at least two EN populations (TableS6), and 18 genes acquired new mutations in only one EN population (TableS5). Appl Environ Microbiol. High groundwater nitrate concentrations inhibit eutrophication of sulphate-rich freshwater wetlands. Tempo and mode of genome evolution in a 50,000-generation experiment. Several mechanisms, including depletion of sulfhydryl groups, reduced biotransformation of nitrates to NO or nitrosothiols, oxygen free radical injury, and downregulation of a membrane-bound enzyme or a nitrate receptor, have been proposed, but the exact mechanism responsible . You have full access to this article via your institution. Internet Explorer). 2012;9:357. The molecular diversity of adaptive convergence. Notably, in this study, parallel evolution was more likely to happen via loss-of-function mutations. Salt stress in. We focused on newly acquired mutations and associated genes in the EN populations, including 119 newly acquired mutations (containing nine large deletions and one insertion predicted using breseq) in 44 genes associated with energy, amino acid, carbohydrate, nucleotide, lipid, and inorganic ion metabolism, cellular process and signal, and information storage and processing (TableS4). Adams J, Rosenzweig F. Experimental microbial evolution: history and conceptual underpinnings. We also used Phyre2 [48] to predict changes in the tertiary structure of HcpR encoded by DVU2547, one of the most frequently mutated genes in EN populations with the highest hits (>99% confidence) for predicted models (Fig. 2017;45:D3628. Lenski RE. The growth of both AN and nitrate-evolved (EN) populations in the LS4D medium with 30mM or 100mM NaNO3 or without additional NaNO3 was measured by a spectrophotometer (Thermo Spectronic 20D+, Waltham, Massachusetts, USA) with three replicates for each population, and OD600 values of all populations were recorded every 23h over a period of 70h. Lag phase was defined as the time after-inoculation to OD600=0.2; growth rate was 2.303 the slope of the linear portion of growth curve by plotting Ln (OD600) as the y-axis and time as the x-axis; biomass yield was the maximum OD600 as previously described [37]. Nitrate tolerance, rebound, and their clinical relevance in stable angina pectoris, unstable angina, and heart failure. Convergent evolution of hyperswarming leads to impaired biofilm formation in pathogenic bacteria. 2003;4:45769. Rodionov DA, Dubchak I, Arkin A, Alm E, Gelfand MS. Reconstruction of regulatory and metabolic pathways in metal-reducing delta-proteobacteria. Mukhopadhyay A, He Z, Alm EJ, Arkin AP, Baidoo EE, Borglin SC, et al. Tenaillon O, Rodriguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, et al. Tolerance is the attenuation, or loss, of one or several of the effects of organic nitrates after long term administration. Ann Intern Med. Genetic complementation was done for all the mutants (ME2394, ME2395, ME2396, ME2405, ME2543, ME2547, and ME2548) and EN7 variant complemented with the plasmid containing a native promoter, ribosome binding site and wild type gene (Table1). Adaptation of Desulfovibrio alaskensis G20 to perchlorate, a specific inhibitor of sulfate reduction. Local migration promotes competitive restraint in a host-pathogen tragedy of the commons. We hypothesized that a set of beneficial genetic changes would emerge in DvH populations after exposure to elevated nitrate (NaNO3) for 1000 generations [22, 23], and that some of these mutations would be parallel among evolved populations [20, 32, 34, 36]. Elseviers Integrated Review Biochemistry (Second Edition). 2015;9:236072. Unable to load your collection due to an error, Unable to load your delegates due to an error. Brief Funct Genomic Proteomic. 4e, f). Every 48h, the OD600 was recorded for each population before transfer (Fig. For example, a previous study indicated a rapid selective sweep of mutations occurred in D. vulgaris populations under NaCl stress within the first 100 generations, and four mutations contributed to shortened lag phases, increased growth rates and biomass yield [23]. Federal government websites often end in .gov or .mil. Nitrate-evolved (EN) populations significantly (p<0.05) increased nitrate tolerance, and whole-genome resequencing identified 119 new mutations in 44 genes of 12 EN populations, among which six functional gene groups were discovered with high mutation frequencies at the population level. Alternatively, iron homeostasis maintained by DVU2571 (feoB) and up-regulation of DVU0598 and DVU0599 encoding carbon starvation proteins regulated by lytR/lytS, which suggested being involved in stresses response as DvH cells transitioned into the stationary phase [66]. 2013;14:75164. Identical frameshift mutation was identified at the coordinate 279997 of DVU0246 in EN1 and EN8, and the same missense mutation occurred at the coordinate 285948 of DVU0251 (Transmembrane protein, tauE like) in EN 7 and EN 12 (Table5). Bender KS, Yen HC, Hemme CL, Yang Z, He Z, He Q, et al. The authors declare that they have no conflict of interest. The complemented strain for ME2548 was not obtained. However, the mechanism of the development of nitrate tolerance is even more complex since it involves neurohormonal counter-regulation, expansion of plasma volume (collectively classified as pseudotolerance), and intrinsic vascular processes defined as true tolerance (Table 2). For example, transcriptomic analysis of DvH showed that elevated nitrate up-regulated key functional genes involved in osmotic, ionic, and nitrite stress responses, and few common patterns of gene expression were observed in response to elevated nitrate, nitrite, or salt [4]. Unauthorized use of these marks is strictly prohibited. Dashed boxes represent possible nitrate tolerance mechanisms. The experimental work of this study (October 2013 to June 2017) was largely supported by ENIGMA-Ecosystems and Networks Integrated with Genes and Molecular Assemblies (http://enigma.lbl.gov), a ScienceFocus Area Program at Lawrence Berkeley National Laboratory is based upon work supported by the U.S. Department of Energy, Office of Science, and Office of Biological & Environmental Research under contract number DE-AC02-05CH11231, the Office of the Vice President for Research at the University of Oklahoma (JZ), and the National Program on Key Basic Research Project of China (973 Program, No. All the primers used in this study are listed in TableS1. Bioinformatics. Disclaimer. In this study, we found shortened lag phase and increased growth rate for EN populations with or without nitrate stress, which is similar to a previous study, showing that both control-evolved populations (EC) and salt-evolved populations (ES) had a shorter lag phase with or without salt stress compared to their ancestral populations (without evolution) in DvH [37]. Second, missense mutations occurred in the other three gene groups, potentially resulting in functional changes in their encoding proteins. In this case, it is reasonable to assume that newly acquired mutations in those GASP-related genes may increase nitrate tolerance through relieving possible environmental stresses like nutrient depletion (Fig. In this gene group, DVU2405 (alcohol dehydrogenase, adh) regulated by a two-component system (DVU2394/DVU2395) was shown to be one of the most highly expressed genes contributing to energy metabolism with different electron donors in DvH [58]. The STRING database in 2017: quality-controlled proteinprotein association networks, made broadly accessible. (i) Nonsense and frameshift mutations were identified in the NSR group of three genes with allele frequencies ranged from 17 to 100% (an average of 72%). All DvH strains used in this study are listed in Table1. Cadby IT, Ibrahim SA, Faulkner M, Lee DJ, Browning D, Busby SJ, et al. Bowles MW, Mogollon JM, Kasten S, Zabel M, Hinrichs KU. Green SJ, Prakash O, Jasrotia P, Overholt WA, Cardenas E, Hubbard D, et al. Elevated nitrate could inhibit sulfate reduction performed by SRB due to its competition for organic electron donors [6], which has a special importance in contaminated or engineered systems since it mitigates sulfide production in the environment [10,11,12]. (a) no stress (LS4D); (b) salt stress (LS4D+100mM NaCl); (c) nitrate stress (LS4D+30mM NaNO3); and (d) the growth phenotype of complemented mutants with extra 30mM NaNO3 in the medium. Genomic DNA (gDNA) of all AN and EN populations was extracted with a GenElute Bacterial Genomic DNA kit (Sigma) following the manufacturers instructions. 1). Also, identical or similar genetic changes (e.g., mutations occurred in same/similar genes with similar phenotypic changes) in replicate populations are considered as a strong indicator of beneficial mutations resulting from stress adaptation in the experimental evolution [31,32,33,34]. Appl Environ Microbiol. Genome Biol. Redox Biol. Before In addition, six mutations were detected in lytR/lytS with the lowest allele frequency (1140% with an average of 19%) among those six gene groups, but all of the mutations were missense except an intergenic mutation at the upstream of DVU0597 start codon in EN3 (TableS9). 2014;49:92431. The NSR group includes three genes: hcp (hybrid cluster protein, DVU2543), hcpR (hcp regulator, DVU2547) and acpD (DVU2548) (Table2). Springer New York: New York, NY; 2014. pp. Experimental evolution of asexual microbial populations coupled with whole-genome resequencing provides a powerful approach to identify adaptive mutations and elucidate genotype-phenotype relationships [20, 21]. In addition, extracellular nitrate concentration of AN and EN populations was measured by ion chromatography (ICS-90A, Dionex, USA). Los DA, Murata N. Membrane fluidity and its roles in the perception of environmental signals. The nitrate cluster genes were proposed to allow non-specific nitrate transport, while transposon mutants of nitrate cluster genes were found to have a growth advantage under nitrate stress [18]. Levy SF, Blundell JR, Venkataram S, Petrov DA, Fisher DS, Sherlock G. Quantitative evolutionary dynamics using high-resolution lineage tracking. J Bacteriol. Long-term survival during stationary phase: evolution and the GASP phenotype. Instead, emerging data suggest that nitrates can cause significant shifts in fluid distribution and secretion of neurohormonal factors that can modulate their vasorelaxant effects. 2011;98:1523. Suri N, Voordouw J, Voordouw G. The effectiveness of nitrate-mediated control of the oil field sulfur cycle depends on the toluene content of the oil. Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities. government site. Springer:Berlin,Germany; 2010. p. 275366. Genomic DNA (gDNA) of all AN and EN populations was extracted with a GenElute Bacterial Genomic DNA kit (Sigma) following the manufacturers instructions. Bender KS, Yen HC, Hemme CL, Yang Z, He Z, He Q, et al. The results demonstrated that nonsense and frameshift mutations in the NSR group (Table3) could improve nitrate tolerance in EN populations. Careers, Unable to load your collection due to an error. Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, et al. 16588. PubMed Ascott MJ, Gooddy DC, Wang L, Stuart ME, Lewis MA, Ward RS, et al. Frequently mutated genes were clustered into six groups (DVU#), including (a) nitrosative stress response (NSR) genes, (b) nitrogen regulation protein C family (NRC) genes, (c) nitrate cluster, (d) fatty acid synthesis genes, (e) iron regulatory genes, and (f) two component system LytR/LytS. CAS Further analyses indicated that a specific nitrate cluster (DVU0245-DVU0251) was related to increased nitrate tolerance, but not for nitrite tolerance in DvH [18], and elevated nitrate and nitrite had distinct effects on inhibition of DvH by mutagenesis [19]. 2015;519:181. FOIA We found that six functional groups with a high frequency of mutations, which were directly or indirectly involved in nitrate tolerance. Identical fixed or nearly fixed missense mutations were also observed at the coordinate 1034711 in DVU0924 in EN4, EN5, and EN9 (TablesS3 and S8). Experimental evolution reveals nitrate tolerance mechanisms in Desulfovibrio vulgaris. Kamp A, Hogslund S, Risgaard-Petersen N, Stief P. Nitrate storage and dissimilatory nitrate reduction by eukaryotic microbes. We focused on newly acquired mutations and associated genes in the EN populations, including 119 newly acquired mutations (containing nine large deletions and one insertion predicted using breseq) in 44 genes associated with energy, amino acid, carbohydrate, nucleotide, lipid, and inorganic ion metabolism, cellular process and signal, and information storage and processing (TableS4). Nat Biotechnol. Also, the same mutation was identified in this group, such as a nonsense mutation in coordinate 2654808 in DVU2543 (Hybrid cluster protein, hcp) in EN4 and EN5, and in position 2660403 of DVU2547 (Hcp regulator, hcpR) in EN7 and EN8 (Table3). Statistical significance of growth parameters was based on the T-test. Temporal transcriptomic analysis as. Environ Sci Technol. Deatherage DE, Barrick JE. The lag phase (a), growth rate (b), and biomass yield (c) of AN and EN populations in LS4D, LS4D+30mM NaNO3, and LS4D+100mM NaNO3 for testing nitrate tolerance. Nonsense and frameshift mutations were identified in NSR, NRC and nitrate clusters, resulting in increased nitrate tolerance through regulating energy metabolism and barring entry of nitrate into DvH cells, while missense mutations in fatty acid synthesis genes, iron regulatory genes, and lytR/lytS may confer general stress tolerance by experimental evolution under elevated nitrate through altering cell membrane characteristics and conferring GASP. Nature. Their lag phase increased while growth rates and biomass gradually decreased as nitrate concentrations increased from 0mM to 30mM (Fig. Acta Med Scand Suppl. Interestingly, eight of ten mutations detected using breseq were located in these three functional groups (NSR, NRC, and nitrate cluster), which were nonsense and frameshift mutations (TableS4). At the gene level (different mutations in the same gene across EN populations), nonsense and frameshift mutations were observed for genes in the NSR, NRC, and nitrate cluster, which may result in nonfunctional proteins and similar phenotypic changes that conferred nitrate tolerance. WITHDRAWN: Trimetazidine for stable angina. Redding AM, Mukhopadhyay A, Joyner DC, Hazen TC, Keasling JD. 2019;21:1395406. 1987 Apr 1;59(8):756-62 The online version of this article (10.1038/s41396-020-00753-5) contains supplementary material, which is available to authorized users. and transmitted securely. 2017;11:2181. Nucleic Acids Res. Clipboard, Search History, and several other advanced features are temporarily unavailable. This study unravels genetic basis of evolutionary changes in nitrate-evolved populations and provides a comprehensive understanding of nitrate tolerance mechanisms, which has important implications for linking genotypes with phenotypes in DvH. PMC Characterization of NaCl tolerance in, Mukhopadhyay A, He Z, Alm EJ, Arkin AP, Baidoo EE, Borglin SC, et al. Received 2020 Mar 12; Revised 2020 Aug 9; Accepted 2020 Aug 17. We found that the gene fabF was high-frequently mutated in EN populations, which could increase unsaturated fatty acid percentages in cell membrane, thus increasing nitrate tolerance possibly by relieving osmotic stress (Fig. To choose a suitable nitrate concentration for our experimental evolution, three ancestral (AN) populations (AN2, AN8, and AN11) were randomly selected and grown under different nitrate concentrations. Also, genetic parallelism is reflected at the mutation, gene, and gene group levels, allowing us to further understand DvH responses to elevated nitrate. In this study, we aimed to understand nitrate tolerance mechanisms in DvH through experimental evolution, which could provide a comprehensive understanding of genetic basis of the adaptation evolution in DvH. https://doi.org/10.1038/s41396-020-00753-5, DOI: https://doi.org/10.1038/s41396-020-00753-5. Therefore, it is expected that experimental evolution and resequencing of whole genomes provide powerful approaches to link genotypes to phenotypes, and explore nitrate tolerance mechanisms in DvH. High-throughput isolation and characterization of untagged membrane protein complexes: outer membrane complexes of. We observed a high frequency of nonsense or frameshift mutations in nitrosative stress response genes (NSR: DVU2543, DVU2547, and DVU2548), nitrogen regulatory protein C family genes (NRC: DVU2394-2396, DVU2402, and DVU2405), and nitrate cluster (DVU0246-0249 and DVU0251). Nat Rev Genet. Google Scholar. Vogwill T, Phillips RL, Gifford DR, MacLean RC. Also, functional gene groups involved in fatty acid synthesis, iron regulation, and two-component system (LytR/LytS) known to be responsive to multiple stresses, had a high frequency of missense mutations. The experimental work of this study (October 2013 to June 2017) was largely supported by ENIGMA-Ecosystems and Networks Integrated with Genes and Molecular Assemblies (http://enigma.lbl.gov), a ScienceFocus Area Program at Lawrence Berkeley National Laboratory is based upon work supported by the U.S. Department of Energy, Office of Science, and Office of Biological & Environmental Research under contract number DE-AC02-05CH11231, the Office of the Vice President for Research at the University of Oklahoma (JZ), and the National Program on Key Basic Research Project of China (973 Program, No. The STRING database in 2017: quality-controlled proteinprotein association networks, made broadly accessible. The growth of parental strain and ME mutants of NSR was tested in LS4D, LS4D+30mM NaNO3 and LS4D+0.15mM NaNO2. Notably, some beneficial mutations occurred in evolved populations may just increase the overall growth (e.g., shortened lag phase, increased growth rate, increased biomass) without direct effects for a specific stress during an experimental evolution [67]. Price MN, Huang KH, Alm EJ, Arkin AP. Also, DVU0249 encodes an outer membrane-associated homodimer [59], and DVU0251 is a TauE like transmembrane protein [18]. To determine if nonsense and frameshift mutations are involved in nitrate tolerance in EN populations and to understand possible nitrate tolerance mechanisms in DvH, we generated representative deletion mutants of NRC and NSR genes, and analyzed their growth under elevated nitrate, NaCl, or nitrite. Callbeck CM, Agrawal A, Voordouw G. Acetate production from oil under sulfate-reducing conditions in bioreactors injected with sulfate and nitrate. We used 12 AN populations (AN1-12) of D. vulgaris Hildenborough (ATCC 29579) from a previous study [37], and a clone of DvH was the founder of 12 populations. Denitrifying bacteria from the genus rhodanobacter dominate bacterial communities in the highly contaminated subsurface of a nuclear legacy waste site. (ii) Among 22 mutations that occurred in the NRC group, 11 nonsense and frameshift mutations were identified in this group with four of them fixed in all EN populations, and the allele frequency of mutations ranged from 11 to 100% with an average of 58% (Table4). doi: 10.1002/14651858.CD003614.pub3. Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities. Kong Y. Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. 2013;79:505968. Seven of 17 mutations in this group were fixed or nearly fixed (>90%), and interestingly, five of them were nonsense and frameshift mutations. and JavaScript. Environmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen University, Guangzhou, 510006, China, Bo Wu,Longfei Shu,Xueqin Yang,Qingyun Yan&Zhili He, Institute for Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, 73019, USA, Bo Wu,Feifei Liu,Aifen Zhou,Megan L. Kempher,Daliang Ning,Feiyan Pan,Joy D. Van Nostrand,Qingyun Yan,Jizhong Zhou&Zhili He, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, State Key Laboratory of Applied Microbiology Southern China, Guangdong Institute of Microbiology, Guangzhou, 510070, China, College of Agronomy, Hunan Agricultural University, Changsha, 410128, China, Departments of Biochemistry and Molecular Microbiology & Immunology, University of Missouri-Columbia, Columbia, MO, 65211, USA, Dpartment des Sciences Biologiques, TOXEN, Ecotoxicology of Aquatic Microorganisms Laboratory, Universit du Qubec Montral, Montral, Canada, State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, 430070, China, State Key Laboratory of Biocatalysis and Enzyme Engineering, Environmental Microbial Technology Center of Hubei Province, College of Life Sciences, Hubei University, Wuhan, 430062, China, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA, School of Environment, Tsinghua University, Beijing, 100084, China, You can also search for this author in Second, missense mutations occurred in the highly contaminated subsurface of a nuclear legacy waste site 18.! 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