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Volume 70, Issue 10

sp. nov. and sp. nov., isolated from the gut of the fungus-growing termite Open Access

Abstract

The taxonomic positions of two novel aerobic, Gram-stain-positive Actinobacteria, designated RB20 and RB56, were determined using a polyphasic approach. Both were isolated from the fungus-farming termite . Results of 16S rRNA gene sequence analysis revealed that both strains are members of the genus with the closest phylogenetic neighbours JCM12860 (98.9 %) and DSM44481 (98.5 %) for RB20 and DSM 44801 (98.3 %), DSM 44290 (98.3 %) and JCM 19832 (98.2 %) for RB56. Digital DNA–DNA hybridization (DDH) between RB20 and JCM12860 and DSM 44481 resulted in similarity values of 33.9 and 22.0 %, respectively. DDH between RB56 and DSM44801 and DSM44290 showed similarity values of 20.7 and 22.3 %, respectively. In addition, wet-lab DDH between RB56 and JCM19832 resulted in 10.2 % (14.5 %) similarity. Both strains showed morphological and chemotaxonomic features typical for the genus , such as the presence of -diaminopimelic acid (Apm) within the cell wall, arabinose and galactose as major sugar components within whole cell-wall hydrolysates, the presence of mycolic acids and major phospholipids (diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol), and the predominant menaquinone MK-8 (H, ω-cyclo). The main fatty acids for both strains were hexadecanoic acid (C), 10-methyloctadecanoic acid (10-methyl C) and -9-octadecenoic acid (C ω9). We propose two novel species within the genus : sp. nov. with the type strain RB20 (=VKM Ac-2841=NRRL B65541) and sp. nov. with the type strain RB56 (=VKM Ac-2842=NRRL B65542).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Macrotermes natalensis , Nocardia and termite gut
Funding
This study was supported by the:
  • V. Kann Rasmussen Foundation (Award VKR10101)
    • Principle Award Recipient: Michael Poulsen
  • Deutsche Forschungsgemeinschaft (Award BE-4799/3-1, ChembioSys A6)
    • Principle Award Recipient: Christine Beemelmanns
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2020-08-20
2024-04-25
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References

  1. Goodfellow M, Maldonado LA. The families Dietziaceae, Gordoniaceae, Nocardiaceae and Tsukamurellaceae . In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. (editors) The Prokaryotes USA: Springer-Verlag; 2006 pp 843–888
     [Google Scholar]
  2. Trevisan V. I generi E Le specie delle battieriacee. 1889; Milan.
  3. Embley TM, Stackebrandt E. The molecular phylogeny and systematics of the actinomycetes. Annu Rev Microbiol 1994; 48:257–289 [View Article][PubMed]
     [Google Scholar]
  4. Demaree JB, Smith NR. Nocardia vaccinii n. sp. causing galls on Blue-berry plants. Phytopathology 1952; 42:249–252
     [Google Scholar]
  5. Kudo T, Hatai K, Seino A. Nocardia seriolae sp. nov. causing nocardiosis of cultured fish. Int J Syst Bacteriol 1988; 38:173–178 [View Article]
     [Google Scholar]
  6. Friedman CS, Beaman BL, Chun J, Goodfellow M, Gee A et al. Nocardia crassostreae sp. nov., the causal agent of nocardiosis in Pacific oysters. Int J Syst Bacteriol 1998; 48:237–246 [View Article][PubMed]
     [Google Scholar]
  7. McNeil MM, Brown JM, Magruder CH, Shearlock KT, Saul RA et al. Disseminated Nocardia transvalensis infection: an unusual opportunistic pathogen in severely immunocompromised patients. J Infect Dis 1992; 165:175–178 [View Article][PubMed]
     [Google Scholar]
  8. Cross T, Rowbotham EN, Mishustin E, Tepper Z, Antoine-Prtaels F et al. Ecology of nocardioform actinomycetes Academic Press; 1976 pp 337–371
     [Google Scholar]
  9. Thawai C, Rungjindamai N, Klanbut K, Tanasupawat S. Nocardia xestospongiae sp. nov., isolated from a marine sponge in the Andaman sea. Int J Syst Evol Microbiol 2017; 67:1451–1456 [View Article][PubMed]
     [Google Scholar]
  10. Xing K, Qin S, Fei S-M, Lin Q, Bian G-K et al. Nocardia endophytica sp. nov., an endophytic actinomycete isolated from the oil-seed plant Jatropha curcas L . Int J Syst Evol Microbiol 2011; 61:1854–1858 [View Article][PubMed]
     [Google Scholar]
  11. Männle D, McKinnie SMK, Mantri SS, Steinke K, Lu Z et al. Comparative Genomics and Metabolomics in the Genus Nocardia . mSystems 2020; 5:e00125–20 [View Article][PubMed]
     [Google Scholar]
  12. Mukai A, Fukai T, Matsumoto Y, Ishikawa J, Hoshino Y et al. Transvalencin Z, a new antimicrobial compound with salicylic acid residue from Nocardia transvalensis IFM 10065. J Antibiot 2006; 59:366–369 [View Article][PubMed]
     [Google Scholar]
  13. Komatsu K, Tsuda M, Shiro M, Tanaka Y, Mikami Y et al. Brasilicardins B-D, new tricyclic terpenoids [correction of terpernoids] from actinomycete Nocardia brasiliensis . Bioorg Med Chem 2004; 12:5545–5551 [View Article][PubMed]
     [Google Scholar]
  14. Kunimoto T, Sawa T, Wakashiro T, Hori M, Umezawa H. Biosynthesis of the formycin family. J Antibiot 1971; 24:253–258 [View Article][PubMed]
     [Google Scholar]
  15. Benndorf R, Guo H, Sommerwerk E, Weigel C, Garcia-Altares M et al. Natural products from Actinobacteria associated with fungus-growing termites. Antibiotics 2018; 7:E83 [View Article][PubMed]
     [Google Scholar]
  16. Ramadhar TR, Beemelmanns C, Currie CR, Clardy J. Bacterial symbionts in agricultural systems provide a strategic source for antibiotic discovery. J Antibiot 2014; 67:53–58 [View Article][PubMed]
     [Google Scholar]
  17. Aanen DK, Eggleton P, Rouland-Lefevre C, Guldberg-Froslev T, Rosendahl S et al. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci U S A 2002; 99:14887–14892 [View Article][PubMed]
     [Google Scholar]
  18. da Costa RR, Hu H, Li H, Poulsen M. Symbiotic plant biomass decomposition in fungus-growing termites. Insects 2019; 10:87 [View Article][PubMed]
     [Google Scholar]
  19. Poulsen M. Towards an integrated understanding of the consequences of fungus domestication on the fungus-growing termite gut microbiota, Environ . Microbiol 2015; 17:2562–2572
     [Google Scholar]
  20. Otani S, Mikaelyan A, Nobre T, Hansen LH, Koné N'Golo A, Koné NA et al. Identifying the core microbial community in the gut of fungus-growing termites. Mol Ecol 2014; 23:4631–4644 [View Article][PubMed]
     [Google Scholar]
  21. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P et al. Artemis: sequence visualization and annotation. Bioinformatics 2000; 16:944–945 [View Article][PubMed]
     [Google Scholar]
  22. Parte AC. LPSN--list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 2014; 42:D613–D616 [View Article][PubMed]
     [Google Scholar]
  23. Meier-Kolthoff JP, Göker M, Spröer C, Klenk H-P. When should a DDH experiment be mandatory in microbial taxonomy?. Arch Microbiol 2013; 195:413–418 [View Article][PubMed]
     [Google Scholar]
  24. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
     [Google Scholar]
  25. Available from http://ggdc.dsmz.de/ .
  26. Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012; 28:1823–1829 [View Article][PubMed]
     [Google Scholar]
  27. 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]
  28. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article][PubMed]
     [Google Scholar]
  29. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article][PubMed]
     [Google Scholar]
  30. Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 1992; 9:678–687 [View Article][PubMed]
     [Google Scholar]
  31. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
     [Google Scholar]
  32. Cui Q, Wang L, Huang Y, Liu Z, Goodfellow M. Nocardia jiangxiensis sp. nov. and Nocardia miyunensis sp. nov., isolated from acidic soils. Int J Syst Evol Microbiol 2005; 55:1921–1925 [View Article][PubMed]
     [Google Scholar]
  33. Tamura T, Ohji S, Ichikawa N, Hosoyama A, Yamazoe A et al. Reclassification of Nocardia species based on whole genome sequence and associated phenotypic data. J Antibiot 2018; 71:633–641 [View Article][PubMed]
     [Google Scholar]
  34. Ruimy R, Riegel P, Carlotti A, Boiron P, Bernardin G et al. Nocardia pseudobrasiliensis sp. nov., a new species of Nocardia which groups bacterial strains previously identified as Nocardia brasiliensis and associated with invasive diseases. Int J Syst Bacteriol 1996; 46:259–264 [View Article][PubMed]
     [Google Scholar]
  35. Yamamura H, Hayakawa M, Nakagawa Y, Tamura T, Kohno T et al. Nocardia takedensis sp. nov., isolated from moat sediment and scumming activated sludge. Int J Syst Evol Microbiol 2005; 55:433–436 [View Article][PubMed]
     [Google Scholar]
  36. Tanasupawat S, Phongsopitanun W, Suwanborirux K, Ohkuma M, Kudo T. Nocardia rayongensis sp. nov., isolated from Thai peat swamp forest soil. Int J Syst Evol Microbiol 2016; 66:1950–1955 [View Article][PubMed]
     [Google Scholar]
  37. Auch AF, Klenk H-P, Göker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2010; 2:142–148 [View Article][PubMed]
     [Google Scholar]
  38. 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]
  39. De Ley J, Cattoir H, Reynaerts A. The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 1970; 12:133–142 [View Article][PubMed]
     [Google Scholar]
  40. Huss VA, Festl H, Schleifer KH. Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol 1983; 4:184–192 [View Article][PubMed]
     [Google Scholar]
  41. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article][PubMed]
     [Google Scholar]
  42. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33:152–155
     [Google Scholar]
  43. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 1987; 37:463–464 [View Article]
     [Google Scholar]
  44. Hasegawa T, Takizawa M, Tanida S. A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 1983; 29:319–322 [View Article]
     [Google Scholar]
  45. Schumann P. Peptidoglycan structure. Meth Microbiol 2011; 38:101–129
     [Google Scholar]
  46. Minnikin DE, Alshamaony L, Goodfellow M. Differentiation of Mycobacterium, Nocardia, and related taxa by thin-layer chromatographic analysis of whole-organism methanolysates. J Gen Microbiol 1975; 88:200–204 [View Article][PubMed]
     [Google Scholar]
  47. Collins MD, Pirouz T, Goodfellow M, Minnikin DE. Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 1977; 100:221–230 [View Article][PubMed]
     [Google Scholar]
  48. Wink J, Schumann P, Atasayar E, Klenk H-P, Zaburannyi N et al. ‘Streptomyces caelicus’, an antibiotic-producing species of the genus Streptomyces, and Streptomyces canchipurensis Li et al. 2015 are later heterotypic synonyms of Streptomyces muensis Ningthoujam et al. 2014. Int J Syst Evol Microbiol 2017; 67:548–556 [View Article]
     [Google Scholar]
  49. Gordon RE, Mihm JM. A comparison of Nocardia asteroides and Nocardia brasiliensis . J Gen Microbiol 1959; 20:129–135 [View Article][PubMed]
     [Google Scholar]
  50. Roth A, Andrees S, Kroppenstedt RM, Harmsen D, Mauch H. Phylogeny of the genus Nocardia based on reassessed 16S rRNA gene sequences reveals underspeciation and division of strains classified as Nocardia asteroides into three established species and two unnamed taxons. J Clin Microbiol 2003; 41:851–856 [View Article][PubMed]
     [Google Scholar]
  51. Minnikin DE, Collins MD, Goodfellow M. Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 1979; 47:87–95 [View Article]
     [Google Scholar]
  52. Collins MD, Jones D. Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2, 4-diaminobutyric acid. J Appl Bacteriol 1980; 48:459–470 [View Article]
     [Google Scholar]
  53. Fatty Acid Analysis Available from. https://www.dsmz.de/services/services-microorganisms/identification/analysis-of-cellular-fatty-acids.html
  54. Kamlage B. Methods for general and molecular bacteriology. In Gerhardt P, Murray RGE, Wood WA, Krieg NR. (editors) 791 pages, numerous figures and tables Washington, DC: American Society for Microbiology; 1994
     [Google Scholar]
  55. Rohde M. Microscopy. In Rainey F, Oren A. (editors) Methods in Microbiology 38, 1st ed. Oxford, UK: Academic Press; 2011 pp 61–100
     [Google Scholar]
  56. Gordon RE, Barnett DA, Handerhan JE, Pang CHN. Nocardia coeliaca, Nocardia autotrophica, and the Nocardin strain. Int J Syst Bacteriol 1974; 24:54–63 [View Article]
     [Google Scholar]
  57. Groth I, Schütze B, Boettcher T, Pullen CB, Rodriguez C et al. Kitasatospora putterlickiae sp. nov., isolated from rhizosphere soil, transfer of Streptomyces kifunensis to the genus Kitasatospora as Kitasatospora kifunensis comb. nov., and emended description of Streptomyces aureofaciens Duggar 1948. Int J Syst Evol Microbiol 2003; 53:2033–2040 [View Article][PubMed]
     [Google Scholar]
  58. Groth I, Schumann P, Rajney FA, Martin K, Schuetze B et al. Bogoriella caseilytica gen. nov., sp. nov., a new alkaliphilic actinomycete from a soda lake in Africa. Int J Syst Bacteriol 1997; 47:788–794 [View Article][PubMed]
     [Google Scholar]
  59. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
     [Google Scholar]
  60. Wink JM. Compendium of actinobacteria methods for the taxonomic description of the actinobacteria. Available at: https://www.dsmz.de/collection/catalogue/microorganisms/special-groups-of-organisms/compendium-of-actinobacteria .
  61. Suter MA. Isolierung und Charakterisierung von Melanin-negativen Mutanten aus Streptomyces glaucescens . Diss. Naturwiss. ETH Zürich, Nr. 6276, 0000 1978
     [Google Scholar]
  62. Xu P, Li W-J, Tang S-K, Zhang Y-Q, Chen G-Z et al. Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family 'Oxalobacteraceae' isolated from China. Int J Syst Evol Microbiol 2005; 55:1149–1153 [View Article][PubMed]
     [Google Scholar]
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Nocardia macrotermitis sp. nov. and Nocardia aurantia sp. nov., isolated from the gut of the fungus-growing termite Macrotermes natalensis
Int J Syst Evol Microbiol 70, 5226 (2020); https://doi.org/10.1099/ijsem.0.004398
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