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Abstract

Three presumptive strains isolated from a high altitude Atacama Desert soil were the subject of a polyphasic study. The isolates, strains 1G4, 1G51 and 1G52, were found to have chemotaxonomic and morphological properties that were consistent with their assignment to the genus . They formed a well supported clade in 16S rRNA gene trees and were most closely related to the type strain of (99.8–99.9% similarity). They were also closely related to the type strains of (99.6 % similarity), (99.7–99.9% similarity), (98.4–99.2% similarity), (99.4–99.5% similarity) and (99.3–99.5% similarity), but were distinguished from their closest relatives by a combination of phenotypic features. Average nucleotide identity and digital DNA:DNA hybridization similarities drawn from comparisons of draft genome sequences of isolate 1G4 and its closest phylogenetic neighbours mentioned above, were well below the threshold used to assign closely related strains to the same species. The close relationship between isolate 1G4 and the type strain of was showed in a phylogenomic tree containing representative strains of family . The draft genome sequence of isolate 1G4 (size 5.18 Kb) was shown to be rich in stress related genes providing further evidence that the abundance of propagules in Atacama Desert habitats reflects their adaptation to the harsh environmental conditions prevalent in this biome. In light of all of these data it is proposed that the isolates be assigned to a novel species in the genus . The name proposed for this taxon is sp. nov., with isolate 1G4 (=DSM 107534=PCM 3003) as the type strain.

Funding
This study was supported by the:
  • Narodowe Centrum Nauki (Award 2017/01/X/NZ8/00140)
    • Principle Award Recipient: Patrycja Golinska
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2020-05-06
2024-04-19
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References

  1. Mevs U, Stackebrandt E, Schumann P, Gallikowski CA, Hirsch P. Modestobacter multiseptatus gen. nov., sp. nov., a budding actinomycete from soils of the Asgard range (Transantarctic Mountains). Int J Syst Evol Microbiol 2000; 50 Pt 1:337–346 [View Article][PubMed][PubMed]
    [Google Scholar]
  2. Normand P, Benson DR. Genus III. Modestobacter Mevs, Stackebrandt, Schumann, Gallikovski and Hirsch 2000, 344AP emend Reddy, Potrafka and Garcia-Pichel 2007, 2018L. In Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I. (editors) Bergey’s Manual of Systematic Bacteriology, 2nd ed., vol. 5, The Actinobacteria, Part A New York: Springer; 2012 pp 536–539
    [Google Scholar]
  3. Golinska P, Montero-Calasanz MDC, Świecimska M, Yaramis A, Igual JM et al. Modestobacter excelsi sp. nov., a novel actinobacterium isolated from a high altitude Atacama Desert soil. Syst Appl Microbiol 2020; 43:126051 [View Article][PubMed][PubMed]
    [Google Scholar]
  4. Montero-Calasanz MDC, Yaramis A, Nouioui I, Igual JM, Spröer C et al. Modestobacter italicus sp. nov., isolated from Carrara marble quarry and emended descriptions of the genus Modestobacter and the species Modestobacter marinus, Modestobacter multiseptatus, Modestobacter roseus and Modestobacter versicolor. Int J Syst Evol Microbiol 2019; 69:1537–1545 [View Article][PubMed][PubMed]
    [Google Scholar]
  5. Normand P. Geodermatophilaceae fam. nov., a formal description. Int J Syst Evol Microbiol 2006; 56:2277–2278 [View Article][PubMed][PubMed]
    [Google Scholar]
  6. Montero-Calasanz MDC, Meier-Kolthoff JP, Zhang D-F, Yaramis A, Rohde M et al. Genome-Scale Data Call for a Taxonomic rearrangement of Geodermatophilaceae . Front Microbiol 2017; 8:2501 [View Article][PubMed][PubMed]
    [Google Scholar]
  7. Sen A, Daubin V, Abrouk D, Gifford I, Berry AM et al. Phylogeny of the class Actinobacteria revisited in the light of complete genomes. The orders 'Frankiales' and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. Int J Syst Evol Microbiol 2014; 64:3821–3832 [View Article][PubMed][PubMed]
    [Google Scholar]
  8. Trujillo ME, Goodfellow M, Busarakam K, Riesco R. Modestobacter lapidis sp. nov. and Modestobacter muralis sp. nov., isolated from a deteriorated sandstone historic building in Salamanca, Spain. Antonie van Leeuwenhoek 2015; 108:311–320 [View Article][PubMed][PubMed]
    [Google Scholar]
  9. Xiao J, Luo Y, Xu J, Xie S, Xu J. Modestobacter marinus sp. nov., a psychrotolerant actinobacterium from deep-sea sediment, and emended description of the genus Modestobacter . Int J Syst Evol Microbiol 2011; 61:1710–1714 [View Article][PubMed][PubMed]
    [Google Scholar]
  10. Busarakam K, Bull AT, Trujillo ME, Riesco R, Sangal V et al. Modestobacter caceresii sp. nov., novel actinobacteria with an insight into their adaptive mechanisms for survival in extreme hyper-arid Atacama Desert soils. Syst Appl Microbiol 2016; 39:243–251 [View Article][PubMed][PubMed]
    [Google Scholar]
  11. Idris H, Goodfellow M, Sanderson R, Asenjo JA, Bull AT. Actinobacterial rare biospheres and dark matter revealed in habitats of the Chilean Atacama desert. Sci Rep 2017; 7:8373 [View Article][PubMed][PubMed]
    [Google Scholar]
  12. Bull AT, Goodfellow M. Dark, rare and inspirational microbial matter in the extremobiosphere: 16 000 M of bioprospecting campaigns. Microbiology 2019; 165:1252–1264 [View Article][PubMed][PubMed]
    [Google Scholar]
  13. Bull AT, Asenjo JA, Goodfellow M, Gómez-Silva B. The Atacama desert: technical resources and the growing importance of novel microbial diversity. Annu Rev Microbiol 2016; 70:215–234 [View Article][PubMed][PubMed]
    [Google Scholar]
  14. Cordero RR, Damiani A, Jorquera J, Sepúlveda E, Caballero M et al. Ultraviolet radiation in the Atacama desert. Antonie van Leeuwenhoek 2018; 111:1301–1313 [View Article][PubMed][PubMed]
    [Google Scholar]
  15. Gómez-Silva B. Lithobiontic life: "Atacama rocks are well and alive". Antonie van Leeuwenhoek 2018; 111:1333–1343 [View Article][PubMed][PubMed]
    [Google Scholar]
  16. Castro JF, Nouioui I, Sangal V, Choi S, Yang S-J et al. Blastococcus atacamensis sp. nov., a novel strain adapted to life in the Yungay core region of the Atacama Desert. Int J Syst Evol Microbiol 2018; 68:2712–2721 [View Article][PubMed][PubMed]
    [Google Scholar]
  17. Castro JF, Nouioui I, Sangal V, Trujillo ME, Montero-Calasanz MDC et al. Geodermatophilus chilensis sp. nov., from soil of the Yungay core-region of the Atacama Desert, Chile. Syst Appl Microbiol 2018; 41:427–436 [View Article][PubMed][PubMed]
    [Google Scholar]
  18. Goodfellow M, Nouioui I, Sanderson R, Xie F, Bull AT. Rare taxa and dark microbial matter: novel bioactive actinobacteria abound in Atacama desert soils. Antonie van Leeuwenhoek 2018; 111:1315–1332 [View Article][PubMed][PubMed]
    [Google Scholar]
  19. Bull AT, Idris H, Sanderson R, Asenjo J, Andrews B et al. High altitude, hyper-arid soils of the Central-Andes harbor mega-diverse communities of actinobacteria. Extremophiles 2018; 22:47–57 [View Article][PubMed][PubMed]
    [Google Scholar]
  20. Vickers JC, Williams ST. An assessment of plate inoculation methods for the enumeration and isolation of soil streptomycetes. Microb Lett 1987; 3:113–117
    [Google Scholar]
  21. Zakharova OS, Zenova GM, Zvyagintsev DG. Some approaches to the selective isolation of actinomycetes of the genus Actinomadura from soil. Microbiology 2003; 72:110–113 [View Article]
    [Google Scholar]
  22. Jones KL. Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 1949; 57:141–145 [View Article][PubMed][PubMed]
    [Google Scholar]
  23. Zhang B-H, Salam N, Cheng J, Li H-Q, Yang J-Y et al. Modestobacter lacusdianchii sp. nov., a phosphate-solubilizing actinobacterium with ability to promote Microcystis growth. PLoS One 2016; 11:e0161069 [View Article][PubMed][PubMed]
    [Google Scholar]
  24. Qin S, Bian G-K, Zhang Y-J, Xing K, Cao C-L et al. Modestobacter roseus sp. nov., an endophytic actinomycete isolated from the coastal halophyte Salicornia europaea Linn., and emended description of the genus Modestobacter . Int J Syst Evol Microbiol 2013; 63:2197–2202 [View Article]
    [Google Scholar]
  25. Reddy GSN, Potrafka RM, Garcia-Pichel F. Modestobacter versicolor sp. nov., an actinobacterium from biological soil crusts that produces melanins under oligotrophy, with emended descriptions of the genus Modestobacter and Modestobacter multiseptatus Mevs et al. 2000. Int J Syst Evol Microbiol 2007; 57:2014–2020 [View Article][PubMed][PubMed]
    [Google Scholar]
  26. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  27. Kelly KL. Central notations for the revised iscc-nbs color-name blocks. J Res Natl Bur Stand 1958; 61:427–431 [View Article]
    [Google Scholar]
  28. Lechevalier MP, Lechevalier HA. The chemotaxonomy of actinomycetes. In Dietz A, Thayer D. (editors) Actinomycete Taxonomy, Special Publication 6 Arlington, VA: Society for Industrial Microbiology; 1980 pp 227–291
    [Google Scholar]
  29. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231 [View Article][PubMed][PubMed]
    [Google Scholar]
  30. Collins MD, Goodfellow M, Minnikin DE, Alderson G. Menaquinone composition of mycolic acid-containing actinomycetes and some sporoactinomycetes. J Appl Bacteriol 1985; 58:77–86 [View Article][PubMed][PubMed]
    [Google Scholar]
  31. Kroppenstedt RM. Fatty acids and menaquinones of actinomycetes and related organisms. In Goodfellow M, Minnikin DE. (editors) Chemical Methods in Bacterial Systematics London: Academic Press; 1985 pp 173–200
    [Google Scholar]
  32. Minnikin DE, O'Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
    [Google Scholar]
  33. Kroppenstedt R, Goodfellow M. The family Thermomonosporaceae: Actinocorallia, Actinomadura, Spirillispora and Thermomonospora . In Dworkin M, Falkow S, Schleifer KH, Stackebrandt E. (editors) The Prokaryotes, Archaea and Bacteria Firmicutes, Actinomycetes 3 New York: Springer; 2006 pp 682–724
    [Google Scholar]
  34. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, MIDI Technical Note 101. Newark: MIDI Inc; 1990
    [Google Scholar]
  35. Golinska P, Ahmed L, Wang D, Goodfellow M. Streptacidiphilus durhamensis sp. nov., isolated from a spruce forest soil. Antonie Van Leeuwenhoek 2013; 104:199–206 [View Article][PubMed][PubMed]
    [Google Scholar]
  36. Golinska P, Wang D, Goodfellow M. Nocardia aciditolerans sp. nov., isolated from a spruce forest soil. Antonie van Leeuwenhoek 2013b; 103:1079–1088 [View Article][PubMed][PubMed]
    [Google Scholar]
  37. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically United database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017a; 67:1613–1617 [View Article][PubMed][PubMed]
    [Google Scholar]
  38. Chun J. Phylogenetic editor (PHYDIT); 1999
  39. 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][PubMed]
    [Google Scholar]
  40. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article][PubMed][PubMed]
    [Google Scholar]
  41. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed][PubMed]
    [Google Scholar]
  42. Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A. How many bootstrap replicates are necessary?. J Comput Biol 2010; 17:337–354 [View Article][PubMed][PubMed]
    [Google Scholar]
  43. Goloboff PA, Farris JS, Nixon KC. TNT, a free program for phylogenetic analysis. Cladistics 2008; 24:774–786 [View Article]
    [Google Scholar]
  44. Swofford D. PAUP*: Phylogenetic Analysis Using Parsimony (* and other methods), ver. 4 Sunderland, MA: Sinauer Associates; 2002
    [Google Scholar]
  45. 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][PubMed]
    [Google Scholar]
  46. 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][PubMed]
    [Google Scholar]
  47. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article][PubMed][PubMed]
    [Google Scholar]
  48. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed][PubMed]
    [Google Scholar]
  49. Versalovic J, Schneider M, De Bruijn FJ, Lupski JR. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 1994; 5:25–40
    [Google Scholar]
  50. Trujillo ME, Alonso-Vega P, Rodríguez R, Carro L, Cerda E et al. The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius . ISME J 2010; 4:1265–1281 [View Article][PubMed][PubMed]
    [Google Scholar]
  51. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed][PubMed]
    [Google Scholar]
  52. Gupta RS, Lo B, Son J. Phylogenomics and comparative genomic studies robustly support division of the genus Mycobacterium into an emended genus Mycobacterium and four novel genera. Front Microbiol 2018; 9:67 [View Article][PubMed][PubMed]
    [Google Scholar]
  53. 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][PubMed]
    [Google Scholar]
  54. Baek I, Lee K, Goodfellow M, Chun J. Comparative Genomic and Phylogenomic Analyses Clarify Relationships Within and Between Bacillus cereus and Bacillus thuringiensis: Proposal for the Recognition of Two Bacillus thuringiensis Genomovars. Front Microbiol 2019; 10:10 [View Article][PubMed][PubMed]
    [Google Scholar]
  55. Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A et al. Assembling genomes and mini-metagenomes from highly chimeric reads. In Deng M, Jiang R, Sun F, Zhang X. (editors) Research in Computational Molecular Biology. RECOMB 2013. Lecture Notes in Computer Science 7821 Berlin, Heidelberg: Springer; 2013 pp 158–170
    [Google Scholar]
  56. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article][PubMed][PubMed]
    [Google Scholar]
  57. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The seed and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:D206–D214 [View Article][PubMed][PubMed]
    [Google Scholar]
  58. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article][PubMed][PubMed]
    [Google Scholar]
  59. Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article][PubMed][PubMed]
    [Google Scholar]
  60. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017b; 110:1281–1286 [View Article][PubMed][PubMed]
    [Google Scholar]
  61. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR, Brenner DJ, Grimont PAD 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]
  62. 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][PubMed]
    [Google Scholar]
  63. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea . Int J Syst Evol Microbiol 2014; 64:316–324 [View Article][PubMed][PubMed]
    [Google Scholar]
  64. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:1–14 [View Article]
    [Google Scholar]
  65. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article][PubMed][PubMed]
    [Google Scholar]
  66. Williams ST, Goodfellow M, Alderson G, Wellington EM, Sneath PH et al. Numerical classification of Streptomyces and related genera. J Gen Microbiol 1983; 129:1743–1813 [View Article][PubMed][PubMed]
    [Google Scholar]
  67. Murray PR, Boron EJ, Pfaller MA, Tenover FC, Yolken RH. Manual of Clinical Microbiology, 7th edn. Washington, DC: ASM Press; 1999
    [Google Scholar]
  68. Vaas LAI, Sikorski J, Michael V, Göker M, Klenk H-P. Visualization and curve-parameter estimation strategies for efficient exploration of phenotype microarray kinetics. PLoS One 2012; 7:e34846 [View Article][PubMed][PubMed]
    [Google Scholar]
  69. Vaas LAI, Sikorski J, Hofner B, Fiebig A, Buddruhs N et al. opm: an R package for analysing OmniLog(R) phenotype microarray data. Bioinformatics 2013; 29:1823–1824 [View Article][PubMed][PubMed]
    [Google Scholar]
  70. Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ et al. antiSMASH 4.0-improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 2017; 45:W36–W41 [View Article][PubMed][PubMed]
    [Google Scholar]
  71. Aziz RK, Devoid S, Disz T, Edwards RA, Henry CS et al. Seed servers: high-performance access to the seed genomes, annotations, and metabolic models. PLoS One 2012; 7:e48053 [View Article][PubMed][PubMed]
    [Google Scholar]
  72. Schultz JE, Matin A. Molecular and functional characterization of a carbon starvation gene of Escherichia coli . J Mol Biol 1991; 218:129–140 [View Article][PubMed][PubMed]
    [Google Scholar]
  73. Lucchetti-Miganeh C, Burrowes E, Baysse C, Ermel G. The post-transcriptional regulator csrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts. Microbiology 2008; 154:16–29 [View Article][PubMed][PubMed]
    [Google Scholar]
  74. Rasmussen JJ, Vegge CS, Frøkiær H, Howlett RM, Krogfelt KA et al. Campylobacter jejuni carbon starvation protein A (CstA) is involved in peptide utilization, motility and agglutination, and has a role in stimulation of dendritic cells. J Med Microbiol 2013; 62:1135–1143 [View Article][PubMed][PubMed]
    [Google Scholar]
  75. Kappes RM, Kempf B, Kneip S, Boch J, Gade J et al. Two evolutionarily closely related ABC transporters mediate the uptake of choline for synthesis of the osmoprotectant glycine betaine in Bacillus subtilis . Mol Microbiol 1999; 32:203–216 [View Article][PubMed][PubMed]
    [Google Scholar]
  76. Mandon K, Osterås M, Boncompagni E, Trinchant JC, Spennato G et al. The Sinorhizobium meliloti glycine betaine biosynthetic genes (betlCBA) are induced by choline and highly expressed in bacteroids. Mol Plant Microbe Interact 2003; 16:709–719 [View Article][PubMed][PubMed]
    [Google Scholar]
  77. Normand P, Gury J, Pujic P, Chouaia B, Crotti E et al. Genome sequence of radiation-resistant Modestobacter marinus strain BC501, a representative actinobacterium that thrives on calcareous stone surfaces. J Bacteriol 2012; 194:4773–4774 [View Article][PubMed][PubMed]
    [Google Scholar]
  78. Li J-song, Bi Y-tian, Dong C, Yang J-feng, Liang W-dong. Transcriptome analysis of adaptive heat shock response of Streptococcus thermophilus . PLoS One 2011; 6:e25777 [View Article][PubMed][PubMed]
    [Google Scholar]
  79. Essoussi I, Ghodhbane-Gtari F, Amairi H, Sghaier H, Jaouani A et al. Esterase as an enzymatic signature of Geodermatophilus adaptability to Sahara desert stones and monuments. J Appl Microbiol 2010; 108:1723–1732 [View Article][PubMed][PubMed]
    [Google Scholar]
  80. Lorite MJ, Tachil J, Sanjuán J, Meyer O, Bedmar EJ. Carbon monoxide dehydrogenase activity in Bradyrhizobium japonicum . Appl Environ Microbiol 2000; 66:1871–1876 [View Article][PubMed][PubMed]
    [Google Scholar]
  81. Montero-Calasanz MdelC, Göker M, Rohde M, Spröer C, Schumann P et al. Chryseobacterium hispalense sp. nov., a plant-growth-promoting bacterium isolated from a rainwater pond in an olive plant nursery, and emended descriptions of Chryseobacterium defluvii, Chryseobacterium indologenes, Chryseobacterium wanjuense and Chryseobacterium gregarium . Int J Syst Evol Microbiol 2013; 63:4386–4395 [View Article][PubMed][PubMed]
    [Google Scholar]
  82. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
    [Google Scholar]
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