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Almeida OGG, Gimenez MP, De Martinis ECP. Comparative pangenomic analyses and biotechnological potential of cocoa-related Acetobacter senegalensis strains. Antonie Van Leeuwenhoek. 2021;doi: 10.1007/s10482-021-01684-7.
Almeida, O. G. G., Gimenez, M. P., & De Martinis, E. C. P. (2021). Comparative pangenomic analyses and biotechnological potential of cocoa-related Acetobacter senegalensis strains. Antonie van Leeuwenhoek, . https://doi.org/10.1007/s10482-021-01684-7
Almeida, O G G, et al. "Comparative pangenomic analyses and biotechnological potential of cocoa-related Acetobacter senegalensis strains." Antonie van Leeuwenhoek vol. (2021). doi: https://doi.org/10.1007/s10482-021-01684-7
Almeida OGG, Gimenez MP, De Martinis ECP. Comparative pangenomic analyses and biotechnological potential of cocoa-related Acetobacter senegalensis strains. Antonie Van Leeuwenhoek. 2021 Nov 24; doi: 10.1007/s10482-021-01684-7. Epub 2021 Nov 24. PMID: 34817761.
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Antonie Van Leeuwenhoek. 2021 Nov 24; doi: 10.1007/s10482-021-01684-7. Epub 2021 Nov 24.

Comparative pangenomic analyses and biotechnological potential of cocoa-related Acetobacter senegalensis strains.

Antonie van Leeuwenhoek

O G G Almeida, M P Gimenez, E C P De Martinis

Affiliations

  1. Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Universidade de São Paulo, Avenida do Café s/n, Ribeirão Preto, São Paulo, 14040-903, Brazil.
  2. Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Universidade de São Paulo, Avenida do Café s/n, Ribeirão Preto, São Paulo, 14040-903, Brazil. [email protected].

PMID: 34817761 DOI: 10.1007/s10482-021-01684-7

Abstract

Acetobacter senegalensis belongs to the group of acetic acid bacteria (AAB) that present potential biotechnological applications, for production of D-gluconate, cellulose and acetic acid. AAB can overcome heat and acid stresses by using strategies involving the overexpression of heat-shock proteins and enzymes from the complex pyrroquinoline-ADH, besides alcohol dehydrogenases (ADH). Nonetheless, the isolation of A. senegalensis and other AAB from food may be challenging due to presence of viable but non-culturable (VBNC) cells and due to uncertainties about nutritional requirements. To contribute for a better understanding of the ecology of AAB, this paper reports on the pangenome analysis of five strains of A. senegalensis recently isolated from a Brazilian spontaneous cocoa fermentation. The results showed biosynthetic clusters exclusively found in some cocoa-related AAB, such as those related to terpene pathways, which are important for flavour development. Genes related to oxidative stress were conserved in all the genomes, with multiple clusters. Moreover, there were genes coding for ADH and putative ABC transporters distributed in core, shell and cloud genomes, while chaperonin-encoding genes were present only in the core and soft-core genomes. Regarding quorum sensing, a response regulator gene was in the shell genome, and the gene encoding for acyl-homoserine lactone efflux protein was in the soft-core genome. There were quorum quenching-related genes, mainly encoding for lactonases, but also for acylases. Moreover, A. senegalensis did not have determinants of virulence or antibiotic resistance, which are good traits for strains intended to be applied in food fermentation.

© 2021. The Author(s), under exclusive licence to Springer Nature Switzerland AG.

Keywords: Acetic acid bacteria; Acetobacter senegalensis; Pangenome analysis

References

  1. Akiko OK, Wang Y, Sachiko K et al (2002) Cloning and characterization of groESL operon in Acetobacter aceti. J Biosci Bioeng 94:140–147. https://doi.org/10.1016/S1389-1723(02)80134-7 - PubMed
  2. Alcock BP, Raphenya AR, Lau TTY et al (2020) CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48:D517–D525. https://doi.org/10.1093/nar/gkz935 - PubMed
  3. Almeida OGG, De Martinis EC (2021) Metagenome-assembled genomes contributes to unravel the microbiome of cocoa fermentation. Appl Environ Microbiol. https://doi.org/10.1128/aem.00584-21 - PubMed
  4. Almeida OGG, Pinto UM, Matos CB et al (2020) Does Quorum Sensing play a role in microbial shifts along spontaneous fermentation of cocoa beans? An in silico perspective. Food Res Int 131:109034. https://doi.org/10.1016/j.foodres.2020.109034 - PubMed
  5. Almeida OGG, Vitulo N, De Martinis ECP, Felis GE (2021) Pangenome analyses of LuxS-coding genes and enzymatic repertoires in cocoa-related lactic acid bacteria. Genomics 113:1659–1670. https://doi.org/10.1016/j.ygeno.2021.04.010 - PubMed
  6. Antipov D, Hartwick N, Shen M et al (2016) PlasmidSPAdes: assembling plasmids from whole genome sequencing data. Bioinformatics 32:3380–3387. https://doi.org/10.1093/bioinformatics/btw493 - PubMed
  7. Aswini K, Gopal NO, Uthandi S (2020) Optimized culture conditions for bacterial cellulose production by Acetobacter senegalensis MA1. BMC Biotechnol 20:1–16. https://doi.org/10.1186/s12896-020-00639-6 - PubMed
  8. Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555. https://doi.org/10.1016/j.mimet.2003.08.009 - PubMed
  9. Blin K, Shaw S, Kloosterman AM et al (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:29–35. https://doi.org/10.1093/nar/gkab335 - PubMed
  10. Brettin T, Davis JJ, Disz T et al (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep. https://doi.org/10.1038/srep08365 - PubMed
  11. Bushnell B (2014) BBTools software package. https://jgi.doe.gov/data-and-tools/bbtools/ - PubMed
  12. Carvalho CC, Phan NN, Chen Y, Reilly PJ (2015) Carbohydrate-binding module tribes. Biopolymers 103:203–214. https://doi.org/10.1002/bip.22584 - PubMed
  13. Chakraborty S, Rani A, Dhillon A, Goyal A (2016) Polysaccharide Lyases. Elsevier, Amsterdam - PubMed
  14. Chen L, Zheng D, Liu B et al (2016) VFDB 2016: hierarchical and refined dataset for big data analysis—10 years on. Nucleic Acids Res 44:D694–D697. https://doi.org/10.1093/nar/gkv1239 - PubMed
  15. Contreras-Moreira B, Vinuesa P (2013) GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl Environ Microbiol 79:7696–7701. https://doi.org/10.1128/AEM.02411-13 - PubMed
  16. De Roos J, De Vuyst L (2018) Acetic acid bacteria in fermented foods and beverages. CurrOpinBiotechnol 49:115–119. https://doi.org/10.1016/j.copbio.2017.08.007 - PubMed
  17. De Roos J, Verce M, Weckx S, De Vuyst L (2020) Temporal Shotgun Metagenomics Revealed the Potential Metabolic Capabilities of Specific Microorganisms During Lambic Beer Production. Front Microbiol. https://doi.org/10.3389/fmicb.2020.01692 - PubMed
  18. Doster E, Lakin SM, Dean CJ et al (2020) MEGARes 2.0: a database for classification of antimicrobial drug, biocide and metal resistance determinants in metagenomic sequence data. Nucleic Acids Res 48:D561–D569. https://doi.org/10.1093/nar/gkz1010 - PubMed
  19. Esquivel-Elizondo S, Ilhan ZE, Garcia-Peña EI, Krajmalnik-Brown R (2017) Insights into Butyrate Production in a Controlled Fermentation System via Gene Predictions. mSystems. https://doi.org/10.1128/msystems.00051-17 - PubMed
  20. Fang G, Rocha EPC, Danchin A (2008) Persistence drives gene clustering in bacterial genomes. BMC Genomics 9:4. https://doi.org/10.1186/1471-2164-9-4 - PubMed
  21. Gao L, Wu X, Xia X, Jin Z (2021) Fine-tuning ethanol oxidation pathway enzymes and cofactor PQQ coordinates the conflict between fitness and acetic acid production by Acetobacter pasteurianus. MicrobBiotechnol 14:643–655. https://doi.org/10.1111/1751-7915.13703 - PubMed
  22. Gautreau G, Bazin A, Gachet M et al (2020) PPanGGOLiN: depicting microbial diversity via a partitioned pangenome graph. PLoS Comput Biol 16:1–27. https://doi.org/10.1371/journal.pcbi.1007732 - PubMed
  23. Gomes RJ, Borges MF, Rosa MF et al (2018) Acetic acid bacteria in the food industry: systematics, characteristics and applications. Food Technol Biotechnol 56:139–151. https://doi.org/10.17113/ftb.56.02.18.5593 - PubMed
  24. Grandclément C, Tannières M, Moréra S et al (2015) Quorum quenching: role in nature and applied developments. FEMS Microbiol Rev 40:86–116. https://doi.org/10.1093/femsre/fuv038 - PubMed
  25. Gupta SK, Padmanabhan BR, Diene SM et al (2014) ARG-annot, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58:212–220. https://doi.org/10.1128/AAC.01310-13 - PubMed
  26. Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086 - PubMed
  27. Hammami R, Zouhir A, Ben Hamida J, Fliss I (2007) BACTIBASE: a new web-accessible database for bacteriocin characterization. BMC Microbiol 7:6–11. https://doi.org/10.1186/1471-2180-7-89 - PubMed
  28. Huang L, Zhang H, Wu P et al (2018) DbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation. Nucleic Acids Res 46:D516–D521. https://doi.org/10.1093/nar/gkx894 - PubMed
  29. Iida A, Ohnishi Y, Horinouchi S (2008) Control of acetic acid fermentation by quorum sensing via N-acylhomoserine lactones in Gluconacetobacter intermedius. J Bacteriol 190:2546–2555. https://doi.org/10.1128/JB.01698-07 - PubMed
  30. Iida A, Ohnishi Y, Horinouchi S (2009) Identification and characterization of target genes of the GinI/GinR quorum-sensing system in Gluconacetobacter intermedius. Microbiology 155:3021–3032. https://doi.org/10.1099/mic.0.028613-0 - PubMed
  31. Ishida T, Sugano Y, Shoda M (2002) Novel glycosyltransferase genes involved in the acetan biosynthesis of Acetobacter xylinum. Biochem Biophys Res Commun 295:230–235. https://doi.org/10.1016/S0006-291X(02)00663-0 - PubMed
  32. Ishikawa M, Okamoto-Kainuma A, Jochi T et al (2010) Cloning and characterization of grpE in Acetobacter pasteurianus NBRC 3283. J Biosci Bioeng 109:25–31. https://doi.org/10.1016/j.jbiosc.2009.07.008 - PubMed
  33. Jakob F, Quintero Y, Musacchio A et al (2019) Acetic acid bacteria encode two levan sucrase types of different ecological relationship. Environ Microbiol 21:4151–4165. https://doi.org/10.1111/1462-2920.14768 - PubMed
  34. Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338. https://doi.org/10.1146/annurev.genet.39.073003.114725 - PubMed
  35. Koul S, Kalia VC (2017) Multiplicity of quorum quenching enzymes: a potential mechanism to limit quorum sensing bacterial population. Indian J Microbiol 57:100–108. https://doi.org/10.1007/s12088-016-0633-1 - PubMed
  36. La China S, Zanichelli G, De Vero L, Gullo M (2018) Oxidative fermentations and exopolysaccharides production by acetic acid bacteria: a mini review. Biotechnol Lett 40:1289–1302. https://doi.org/10.1007/s10529-018-2591-7 - PubMed
  37. Letunic I, Bork P (2019) Interactive Tree of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47:256–259. https://doi.org/10.1093/nar/gkz239 - PubMed
  38. Levasseur A, Drula E, Lombard V et al (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:1–14. https://doi.org/10.1186/1754-6834-6-41 - PubMed
  39. Liu LP, Huang LH, Ding XT et al (2019) Identification of quorum-sensing molecules of N-acyl-homoserine lactone in Gluconacetobacter strains by liquid chromatography-tandem mass spectrometry. Molecules 24:2694. https://doi.org/10.3390/molecules24152694 - PubMed
  40. Lynch KM, Zannini E, Wilkinson S et al (2019) Physiology of acetic acid bacteria and their role in vinegar and fermented beverages. Compr Rev Food Sci Food Saf 18:587–625. https://doi.org/10.1111/1541-4337.12440 - PubMed
  41. Martínez-Núñez MA, López VEL (2016) Nonribosomal peptides synthetases and their applications in industry. Sustain Chem Process 4:1–8. https://doi.org/10.1186/s40508-016-0057-6 - PubMed
  42. Matsutani M, Hirakawa H, Nishikura M et al (2011) Increased number of Arginine-based salt bridges contributes to the thermotolerance of thermotolerant acetic acid bacteria, Acetobacter tropicalis SKU1100. Biochem Biophys Res Commun 409:120–124. https://doi.org/10.1016/j.bbrc.2011.04.126 - PubMed
  43. Nakamura AM, Nascimento AS, Polikarpov I (2017) Structural diversity of carbohydrate esterases. Biotechnol Res Innov 1:35–51. https://doi.org/10.1016/j.biori.2017.02.001 - PubMed
  44. Nakano S, Fukaya M (2008) Analysis of proteins responsive to acetic acid in Acetobacter: Molecular mechanisms conferring acetic acid resistance in acetic acid bacteria. Int J Food Microbiol 125:54–59. https://doi.org/10.1016/j.ijfoodmicro.2007.05.015 - PubMed
  45. Naseeb S, Ames RM, Delneri D, Lovell SC (2017) Rapid functional and evolutionary changes follow gene duplication in yeast. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.1393 - PubMed
  46. Nayfach S, Shi ZJ, Seshadri R et al (2019) New insights from uncultivated genomes of the global human gut microbiome. Nature 568:505–510. https://doi.org/10.1038/s41586-019-1058-x - PubMed
  47. Ndoye B, Cleenwerck I, Engelbeen K et al (2007) Acetobacter senegalensis sp. nov., a thermotolerant acetic acid bacterium isolated in Senegal (sub-Saharan Africa) from mango fruit (Mangifera indica L.). Int J Syst Evol Microbiol 57:1576–1581. https://doi.org/10.1099/ijs.0.64678-0 - PubMed
  48. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222. https://doi.org/10.1146/annurev-genet-102108-134304 - PubMed
  49. Pal C, Bengtsson-Palme J, Rensing C et al (2014) BacMet: Antibacterial biocide and metal resistance genes database. Nucleic Acids Res 42:737–743. https://doi.org/10.1093/nar/gkt1252 - PubMed
  50. Pelicaen R, Gonze D, Teusink B et al (2019) Genome-scale metabolic reconstruction of Acetobacter pasteurianus 386B, a candidate functional starter culture for cocoa bean fermentation. Front Microbiol. https://doi.org/10.3389/fmicb.2019.02801 - PubMed
  51. Pritchard L, Glover RH, Humphris S et al (2016) Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 8:12–24. https://doi.org/10.1039/c5ay02550h - PubMed
  52. Prjibelski A, Antipov D, Meleshko D et al (2020) Using SP Ades de novo assembler. Curr Protoc Bioinforma 70:1–29. https://doi.org/10.1002/cpbi.102 - PubMed
  53. Qiu X, Zhang Y, Hong H (2021) Classification of acetic acid bacteria and their acid resistant mechanism. AMB Express 11:29. https://doi.org/10.1186/s13568-021-01189-6 - PubMed
  54. Ruiz-Perez CA, Conrad RE, Konstantinidis KT (2021) MicrobeAnnotator: a user-friendly, comprehensive functional annotation pipeline for microbial genomes. BMC Bioinform 22:1–16. https://doi.org/10.1186/s12859-020-03940-5 - PubMed
  55. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153 - PubMed
  56. Seemann T Abricate. https://github.com/tseemann/abricate - PubMed
  57. Shafiei R, Delvigne F, Babanezhad M, Thonart P (2013) Evaluation of viability and growth of Acetobacter senegalensis under different stress conditions. Int J Food Microbiol 163:204–213. https://doi.org/10.1016/j.ijfoodmicro.2013.03.011 - PubMed
  58. Shafiei R, Zarmehrkhorshid R, Mounir M et al (2017) Influence of carbon sources on the viability and resuscitation of Acetobacter senegalensis during high-temperature gluconic acid fermentation. Bioprocess Biosyst Eng 40:769–780. https://doi.org/10.1007/s00449-017-1742-x - PubMed
  59. Shafiei R, Leprince P, Sombolestani AS et al (2019) Effect of sequential acclimation to various carbon sources on the proteome of Acetobacter senegalensis LMG 23690 - PubMed
  60. Siedenburg G, Jendrossek D (2011) Squalene-hopene cyclases. Appl Environ Microbiol 77:3905–3915. https://doi.org/10.1128/AEM.00300-11 - PubMed
  61. Simão FA, Waterhouse RM, Ioannidis P et al (2015) BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212. https://doi.org/10.1093/bioinformatics/btv351 - PubMed
  62. Son H-J, Heo M-S, Kim Y-G, Lee S-J (2001) Optimization of fermentation conditions for the production of bacterial cellulose by a newly isolated Acetobacter sp.A9 in shaking cultures. Biotechnol Appl Biochem 33:1. https://doi.org/10.1042/ba20000065 - PubMed
  63. Subramoni S, Venturi V (2009) LuxR-family “solos”: Bachelor sensors/regulators of signalling molecules. Microbiology 155:1377–1385. https://doi.org/10.1099/mic.0.026849-0 - PubMed
  64. Tran TN, Phong HX, ThaoAnh BT et al (2018) High-temperature production of acerola vinegar using thermotolerant Acetobacter senegalensis A28. Vietnam J Sci Technol Eng 60:13–18. https://doi.org/10.31276/vjste.60(3).13 - PubMed
  65. Trček J, Dogsa I, Accetto T, Stopar D (2021) Acetan and acetan-like polysaccharides: genetics, biosynthesis, structure, and viscoelasticity. Polymers (basel) 13:1–16. https://doi.org/10.3390/polym13050815 - PubMed
  66. Valera MJ, Mas A, Streit WR, Mateo E (2016) GqqA, a novel protein in Komagataeibacter europaeus involved in bacterial quorum quenching and cellulose formation. Microb Cell Fact 15:1–15. https://doi.org/10.1186/s12934-016-0482-y - PubMed
  67. Versalovic J, Schneider M, De Bruijn FJ, Lupski J (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40 - PubMed
  68. Vinuesa P, Ochoa-Sánchez LE, Contreras-Moreira B (2018) GET_PHYLOMARKERS, a software package to select optimal orthologous clusters for phylogenomics and inferring pan-genome phylogenies, used for a critical geno-taxonomic revision of the genus Stenotrophomonas. Front Microbiol 9:1–22. https://doi.org/10.3389/fmicb.2018.00771 - PubMed
  69. Wang B, Shao Y, Chen T et al (2015a) Global insights into acetic acid resistance mechanisms and genetic stability of Acetobacter pasteurianus strains by comparative genomics. Sci Rep 5:1–14. https://doi.org/10.1038/srep18330 - PubMed
  70. Wang Z, Zang N, Shi J et al (2015b) Comparative proteome of Acetobacter pasteurianus Ab3 during the high acidity rice vinegar fermentation. Appl Biochem Biotechnol 177:1573–1588. https://doi.org/10.1007/s12010-015-1838-1 - PubMed
  71. Wu JJ, Ma YK, Zhang FF, Chen FS (2012) Biodiversity of yeasts, lactic acid bacteria and acetic acid bacteria in the fermentation of “Shanxi aged vinegar”, a traditional Chinese vinegar. Food Microbiol 30:289–297. https://doi.org/10.1016/j.fm.2011.08.010 - PubMed
  72. Xia K, Zang N, Zhang J et al (2016) New insights into the mechanisms of acetic acid resistance in Acetobacter pasteurianus using iTRAQ-dependent quantitative proteomic analysis. Int J Food Microbiol 238:241–251. https://doi.org/10.1016/j.ijfoodmicro.2016.09.016 - PubMed
  73. Xia K, Han C, Xu J, Liang X (2020) Transcriptome response of Acetobacter pasteurianus Ab3 to high acetic acid stress during vinegar production. Appl Microbiol Biotechnol 104:10585–10599. https://doi.org/10.1007/s00253-020-10995-0 - PubMed
  74. Yang H, Yu Y, Fu C, Chen F (2019) Bacterial acid resistance toward organic weak acid revealed by RNA-seq transcriptomic analysis in Acetobacter pasteurianus. Front Microbiol 10:1–14. https://doi.org/10.3389/fmicb.2019.01616 - PubMed
  75. Yin H, Zhang R, Xia M et al (2017) Effect of aspartic acid and glutamate on metabolism and acid stress resistance of Acetobacter pasteurianus. Microb Cell Fact 16:1–14. https://doi.org/10.1186/s12934-017-0717-6 - PubMed
  76. Zankari E, Hasman H, Cosentino S et al (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644. https://doi.org/10.1093/jac/dks261 - PubMed
  77. Zhang Z, Ma H, Yang Y et al (2015) Protein profile of Acetobacter pasteurianus HSZ3-21. CurrMicrobiol 70:724–729. https://doi.org/10.1007/s00284-015-0777-y - PubMed

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