1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 71, Issue 5

gen. nov., sp. nov, a haloalkaliphilic actinobacterium from a soda solonchak soil Open Access

Abstract

A haloalkaliphilic hydrolytic actinobacterium, strain ACPA22, was enriched and isolated in pure culture from saline alkaline soil (soda solonchak) in northeastern Mongolia. The isolate was facultatively alkaliphilic, growing at pH 6.5–10.5 (optimum at 7.3–9.0) and highly salt-tolerant, tolerating up to 3 M total Na as carbonates. The hydrolytic nature of ACPA22 was confirmed by two different growth-dependent methods and by the presence of multiple glycosidase-encoding genes in the genome. The 16S rRNA gene-based phylogenetic analysis demonstrated that strain ACPA22 formed a deep-branching lineage within the family with the highest sequence similarity value to 18 (92.1 %) and Miq-4 (91.8 %). The average amino acid identity values (56.1–61.5 %) between ACPA22 and other members with available genomes did not exceed the threshold reported for different genera. The cell wall of ACPA22 contained -diaminopimelic acid, glycine, glutamic acid and alanine in a molar ratio, characteristic of the peptidoglycan type A1γ'. The whole-cell sugars included mannose, galactose, arabinose, ribose and xylose. The major menaquinones were MK-10(Н) and MK-11(Н). The identified polar lipids were represented by phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylinositol and phosphatidylinositol mannosides. In addition, the strain had a few unidentified characteristic polar lipids, including an amine-containing phospholipid with chromatographic mobility similar to that of phosphatidylinositol. The polar lipid fatty acids were dominated by anteiso-C and iso-C. The genome included a chromosome of 3.94 Mbp (G+C content 61.5 mol%) encoding 3285 proteins and two plasmids of 59.8 and 14.8 kBp. Based on the data obtained in this study, a new genus and species, gen. nov., sp. nov, is proposed with the type strain ACPA22 (=DSM 106290=VKM Ac-2771).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Glycomycetaceae , haloalkaliphilic , hydrolytic , Natronoglycomyces and soda solonchak soil
Funding
This study was supported by the:
  • Russian Ministry of Higher Education and Science
    • Principle Award Recipient: IlyaV. Kublanov
  • Russian Ministry of Higher Education and Science
    • Principle Award Recipient: LyudmilaI. Evtushenko
  • Russian Ministry of Higher Education and Science
    • Principle Award Recipient: AlexanderG. Elcheninov
  • Russian Ministry of Higher Education and Science
    • Principle Award Recipient: TatjanaV. Khijniak
  • Russian Ministry of Higher Education and Science
    • Principle Award Recipient: DimitryY Sorokin
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004804
2021-05-17
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/5/ijsem004804.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004804&mimeType=html&fmt=ahah

References

  1. Kondorskaya NI. Geographic distribution of soda soils in USSR. Soil Sci 1965; 9:10–16
     [Google Scholar]
  2. Antony-Babu S, Goodfellow M. Biosystematics of alkaliphilic streptomycetes isolated from seven locations across a beach and dune sand system. Antonie van Leeuwenhoek 2008; 94:581–591 [View Article][PubMed]
     [Google Scholar]
  3. Ronoh RC, Budambula NLM, Mwirichia RK, Boga HI. Isolation and characterization of actinobacteria from Lake Magadi, Kenya. African J Microbiol Res 2013; 7:4200–4206
     [Google Scholar]
  4. Grant WD, Jones BE. Bacteria, archaea and viruses of soda lakes. In Schagerl M. editor Soda lakes of East Africa Switzerland: Springer International Publishing; 2016 pp 97–147
     [Google Scholar]
  5. Mwirichia R, Muigai AW, Tindall B, Boga HI, Stackebrandt E. Isolation and characterisation of bacteria from the haloalkaline lake Elmenteita, Kenya. Extremophiles 2010; 14:339–348 [View Article][PubMed]
     [Google Scholar]
  6. Ara I, Daram D, Baljinova T, Yamamura H, Hozzein WN. Isolation, classification, phylogenetic analysis and scanning electron microscopy of halophilic, halotolerant and alkaliphilic actinomycetes isolated from hypersaline soil. African J Microbiol Res 2013; 7:298–308
     [Google Scholar]
  7. Sorokin DY, Khijniak TV, Kolganova TV, Jones BE, Kublanov IV. Culturable diversity of aerobic polyhydrolytic haloalkaliphilic bacteria in saline alkaline soils. Peer J 2017; 5:e3796
     [Google Scholar]
  8. Nigam PS. Microbial enzymes with special characteristics for biotechnological applications. Biomolecules 2013; 3:597–611 [View Article][PubMed]
     [Google Scholar]
  9. Chinnathambi A. Industrial important enzymes from alkaliphiles – an overview. Biosci Biotechnol Res Asia 2015; 12:2007–2016 [View Article]
     [Google Scholar]
  10. Shivlata L, Satyanarayana T. Thermophilic and alkaliphilic Actinobacteria: biology and potential applications. Front Microbiol 2015; 6:1014 [View Article][PubMed]
     [Google Scholar]
  11. Stackebrandt E, Rainey FA, Ward-Rainey NL. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Evol Microbiol 1997; 47:479–491
     [Google Scholar]
  12. Zhi X-Y, Li W-J, Stackebrandt E. An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol 2009; 59:589–608 [View Article][PubMed]
     [Google Scholar]
  13. Labeda DP. Order VII. Glycomycetales ord. Nov. Goodfellow M, Kampfer P, Busse H, Trujillo M, Suzuki K. eds In Bergey’s Manual of Systematic Bacteriology, 2nd ed. edn Vol 5 Berlin: Springer; 2012 p 546
     [Google Scholar]
  14. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 2018; 9:9 [View Article][PubMed]
     [Google Scholar]
  15. Salam N, Jiao J-Y, Zhang X-T, Li W-J. Update on the classification of higher ranks in the phylum Actinobacteria. Int J Syst Evol Microbiol 2020; 70:1331–1355 [View Article][PubMed]
     [Google Scholar]
  16. Labeda DP, Testa RT, Lechevalier MP. Lechevalier HA. Glycomyces, a new genus of the Actinomycetales. Int J Syst Bacteriol 1985; 35:417–421
     [Google Scholar]
  17. Labeda DP, Kroppenstedt RM. Emended description of the genus Glycomyces and description of Glycomyces algeriensis sp. nov., Glycomyces arizonensis sp. nov. and Glycomyces lechevalierae sp. nov. Int J Syst Evol Microbiol 2004; 54:2343–2346 [View Article][PubMed]
     [Google Scholar]
  18. Labeda DP, Kroppenstedt RM. Stackebrandtia nassauensis gen. nov., sp. nov. and emended description of the family Glycomycetaceae. Int J Syst Evol Microbiol 2005; 55:1687–1691 [View Article][PubMed]
     [Google Scholar]
  19. Guan T-W, Tang S-K, Wu J-Y, Zhi X-Y, Xu L-H et al. Haloglycomyces albus gen. nov., sp. nov., a halophilic, filamentous actinomycete of the family Glycomycetaceae. Int J Syst Evol Microbiol 2009; 59:1297–1301 [View Article][PubMed]
     [Google Scholar]
  20. Moshtaghi Nikou M, Ramezani M, Ali Amoozegar M, Rasouli M, Abolhassan Shahzadeh Fazeli S et al. Salininema proteolyticum gen. nov., sp. nov., a halophilic rare actinomycete isolated from wetland soil, and emended description of the family Glycomycetaceae. Int J Syst Evol Microbiol 2015; 65:3727–3733 [View Article][PubMed]
     [Google Scholar]
  21. XJ L, Liu JM, Wu Y, Zhang WM, Li J. Description of Salilacibacter albus gen. nov., sp. nov., isolated from a dried salt lake, and reclassification of Paraglycomyces xinjiangensis Luo, et al. 2015 as a later heterotypic synonym of Salininema proteolyticum Nikou, et al. 2015 with emended descriptions of the genus Salininema and Salininema proteolyticum. Int J Syst Evol Microbiol 2016:2558–2565
     [Google Scholar]
  22. Lv L-L, Zhang Y-F, Zhang L-L. Glycomyces tarimensis sp. nov., an actinomycete isolated from a saline-alkali habitat. Int J Syst Evol Microbiol 2015; 65:1587–1591 [View Article][PubMed]
     [Google Scholar]
  23. Guan T-W, Xia Z-F, Xiao J, Wu N, Chen Z-J et al. Glycomyces halotolerans sp. nov., a novel actinomycete isolated from a hypersaline habitat in Xinjiang, China. Antonie van Leeuwenhoek 2011; 100:137–143 [View Article][PubMed]
     [Google Scholar]
  24. Guan T-W, Wang P-H, Tian L, Tang S-K, Xiang H-P. Glycomyces lacisalsi sp. nov., an actinomycete isolated from a hypersaline habitat. Int J Syst Evol Microbiol 2016; 66:5366–5370 [View Article][PubMed]
     [Google Scholar]
  25. Han X-X, Luo X-X, Zhang L-L. Glycomyces fuscus sp. nov. and Glycomyces albus sp. nov., actinomycetes isolated from a hypersaline habitat. Int J Syst Evol Microbiol 2014; 64:2437–2441 [View Article][PubMed]
     [Google Scholar]
  26. Mohammadipanah F, Atasayar E, Heidarian S, Wink J. Glycomyces sediminimaris sp. nov., a new species of actinobacteria isolated from marine sediment. Int J Syst Evol Microbiol 2018; 68:2357–2363 [View Article][PubMed]
     [Google Scholar]
  27. Zhang W-Q, Li Y-Q, Liu L, Salam N, Fang B-Z et al. Stackebrandtia cavernae sp. nov., a novel actinobacterium isolated from a karst cave sample. Int J Syst Evol Microbiol 2016; 66:1206–1211 [View Article][PubMed]
     [Google Scholar]
  28. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340
     [Google Scholar]
  29. Reasoner DJ, Geldreich EE. A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 1985; 49:1–7 [View Article][PubMed]
     [Google Scholar]
  30. Huang Y, Goodfellow M. Pseudonocardia. Bergey’s Manual of Systematics of Archaea and Bacteria 2015 pp 1–32
     [Google Scholar]
  31. Boone CJ, Pine L. Rapid method for characterization of actinomycetes by cell wall composition. Appl Microbiol 1968; 16:279–284[PubMed]
     [Google Scholar]
  32. Moore S, Stein WH. Chromatographic determination of amino acids by the use of automatic recording equipment. Methods Enzymol 1963; 6:819–831
     [Google Scholar]
  33. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231[PubMed]
     [Google Scholar]
  34. Sinner M, Puls J. Non-Corrosive dye reagent for detection of reducing sugars in borate complex ion-exchange chromatography. J Chromatogr A 1978; 156:197–204 [View Article]
     [Google Scholar]
  35. Collins MD, Jones D. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol Rev 1981; 45:316–354[PubMed]
     [Google Scholar]
  36. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G. A et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241
     [Google Scholar]
  37. Da Costa MS, Albuquerque L, Nobre MF, Wait R. The identification of polar lipids in prokaryotes. Methods in Microbiology 2011; 38:165–181
     [Google Scholar]
  38. Kudryashova EB, Karlyshev AV, Ariskina EV, Streshinskaya GM, Vinokurova NG et al. Cohnella kolymensis sp. nov., a novel bacillus isolated from Siberian permafrost. Int J Syst Evol Microbiol 2018; 68:2912–2917 [View Article][PubMed]
     [Google Scholar]
  39. Evtushenko LI, Taptykova SD, Akimov VN, Semyonova SA, Kalakoutskii LV. Glycomyces tenuis sp. nov. Int J Syst Bacteriol 1991; 41:154–157
     [Google Scholar]
  40. Labeda DP. Glycomycetaceae. In Whitman WB. editor Bergey’s Manual of Systematic of Bacteria and Archaea Chichester: Wiley; published on line: 14 September 2015
     [Google Scholar]
  41. Schumann P. Peptidoglycan structure. Methods in Microbiology 2011; 38:101–129
     [Google Scholar]
  42. Wang Y-X, Zhi X-Y, Zhang Y-Q, Cui X-L, Xu L-H et al. Stackebrandtia albiflava sp. nov. and emended description of the genus Stackebrandtia. Int J Syst Evol Microbiol 2009; 59:574–577 [View Article][PubMed]
     [Google Scholar]
  43. Liu M-J, Jin C-Z, Park D-J, Asem MD, Xiao M et al. Stackebrandtia soli sp. nov., a novel actinobacterium isolated from a soil sample. Int J Syst Evol Microbiol 2018; 68:1215–1219 [View Article][PubMed]
     [Google Scholar]
  44. Zhang X, Ren K, Du J, Liu H, Zhang L. Glycomyces artemisiae sp. nov., an endophytic actinomycete isolated from the roots of Artemisia argyi. Int J Syst Evol Microbiol 2014; 64:3492–3495 [View Article][PubMed]
     [Google Scholar]
  45. Wang Y, Luo X-X, Xia Z-F, Wan C-X, Alim A et al. Glycomyces xiaoerkulensis sp. nov., isolated from Xiaoerkule lake in Xinjiang, China. Int J Syst Evol Microbiol 2018; 68:2722–2726 [View Article][PubMed]
     [Google Scholar]
  46. Park D. Genomic DNA isolation from different biological materials. Methods in Molecular Biology 2007 pp 3–13
     [Google Scholar]
  47. Cashion P, Holder-Franklin MA, McCully J, Franklin M. A rapid method for the base ratio determination of bacterial DNA. Anal Biochem 1977; 81:461–466 [View Article][PubMed]
     [Google Scholar]
  48. Mesbah M, Premachandran U, Whitman WB. Precise measurement of the G + C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 1989; 39:159–167
     [Google Scholar]
  49. Tamaoka J, Komagata K. Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 1984; 25:125–128
     [Google Scholar]
  50. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20171–7
     [Google Scholar]
  51. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
     [Google Scholar]
  52. Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2017; 2:1533–1542 [View Article][PubMed]
     [Google Scholar]
  53. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article][PubMed]
     [Google Scholar]
  54. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article][PubMed]
     [Google Scholar]
  55. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
     [Google Scholar]
  56. Letunic I, Bork P. Interactive tree of life (iTOL) V4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article][PubMed]
     [Google Scholar]
  57. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: Soft-rotting enterobacterial plant pathogens. Anal Methods 2016; 8:12–24
     [Google Scholar]
  58. Rodriguez-R L, Konstantinidis K. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Prepr 2016; 4:e1900v1
     [Google Scholar]
  59. Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J 2017; 11:2399–2406 [View Article][PubMed]
     [Google Scholar]
  60. Sorokin DY. Is there a limit for high-pH life?. Int J Syst Evol Microbiol 2005; 55:1405–1406 [View Article][PubMed]
     [Google Scholar]
  61. Panschin I, Becher M, Verbarg S, Spröer C, Rohde M et al. Description of Gramella forsetii sp. nov., a marine isolated from North Sea water, and emended description of Gramella gaetbulicola Cho, et al. 2011. Int J Syst Evol Microbiol 2017:697–703
     [Google Scholar]
  62. Zhang H, Yohe T, Huang L, Entwistle S, Wu P et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2018; 46:W95–W101 [View Article][PubMed]
     [Google Scholar]
  63. Dong L, Salam N, W-J L. Haloglycomyces. Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons, Inc; 2020
     [Google Scholar]
  64. Parte AC. LPSN - List of Prokaryotic names with Standing in Nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 2018; 68:1825–1829 [View Article][PubMed]
     [Google Scholar]
  65. Qin S, Wang H-B, Chen H-H, Zhang Y-Q, Jiang C-L et al. Glycomyces endophyticus sp. nov., an endophytic actinomycete isolated from the root of Carex baccans Nees. Int J Syst Evol Microbiol 2008; 58:2525–2528 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004804
Loading
Natronoglycomyces albus gen. nov., sp. nov, a haloalkaliphilic actinobacterium from a soda solonchak soil
Int J Syst Evol Microbiol 71, 004804 (2021); https://doi.org/10.1099/ijsem.0.004804
/content/journal/ijsem/10.1099/ijsem.0.004804
/content/journal/ijsem/10.1099/ijsem.0.004804
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error