Abstract
In this study, two endophytic bacterial strains designated JS21-1T and S6-262T isolated from leaves of Elaeis guineensis and stem tissues of Jatropha curcas respectively, were subjected for polyphasic taxonomic approach. On R2A medium, colonies of strains JS21-1T and S6-262T are orange and yellow, respectively. Phylogenetic analyses using 16S rRNA gene sequencing and whole-genome sequences placed the strains in distinct clades but within the genus Sphingomonas. The DNA G + C content of JS21-1T and S6-262T were 67.31 and 66.95%, respectively. Furthermore, the average nucleotide identity and digital DNA-DNA hybridization values of strains JS21-1T and S6-262T with phylogenetically related Sphingomonas species were lower than 95% and 70% respectively. The chemotaxonomic studies indicated that the major cellular fatty acids of the strain JS21-1T were summed feature 8 (C18:1 ω7c and/or C18:1 ω6c), C16:0, and C14:0 2OH; strain S6-262T possessed summed feature 3 (C16:1 ω7c and/or iso-C15:0 2-OH) and summed feature 8 (C18:1 ω6c and/or C18:1 ω7c). The major quinone was Q10, and the unique polyamine observed was homospermidine. The polar lipid profile comprised of mixture of sphingoglycolipid, phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol and certain uncharacterised phospholipids and lipids. Based on this polyphasic evidence, strains JS21-1T and S6-262T represent two novel species of the genus Sphingomonas, for which the names Sphingomonas palmae sp. nov. and Sphingomonas gellani sp. nov. are proposed, respectively. The type strain of Sphingomonas palmae sp. nov. is JS21-1T (= DSM 27348T = KACC 17591T) and the type strain of Sphingomonas gellani sp. nov. is S6-262T (= DSM 27346T = KACC 17594T).
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Anzai Y, Kim H, Park J-Y, Wakabayashi H, Oyaizu H (2000) Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int J Syst Evol Microbiol 50:1563–1589
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75
Bennett S (2004) Solexa ltd. Pharmacogenomics 5:433–438
Blom J, Albaum SP, Doppmeier D, Pühler A, Vorhölter FJ, Zakarzewski M, Goesmann A (2009) EDGAR: a software framework for the comparitive analysis of prokaryotic genomes. BMC Bioinformatics 20:154
Blom J, Kreis J, Spanig S, Juhre T, Bertelli C, Ernst C (2016) Goesmann A EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res 44(W1):W22–W28
Busse J, Auling G (1988) Polyamine pattern as a chemotaxonomic marker within the Proteobacteria. Syst Appl Microbiol 11:1–8
Busse HJ, Kämpfer P, Denner EB (1999) Chemotaxonomic characterisation of Sphingomonas. J Ind Microbiol Biotechnol 23:242–251
Busse H-J, Denner EB, Buczolits S, Salkinoja-Salonen M, Bennasar A, Kämpfer P (2003) Sphingomonas aurantiaca sp. nov., Sphingomonas aerolata sp. nov. and Sphingomonas faeni sp. nov., air-and dustborne and Antarctic, orange-pigmented, psychrotolerant bacteria, and emended description of the genus Sphingomonas. Int J Syst Evol Microbiol 53:1253–1260
Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973
Cappuccino J, Welsh C (2018) Microbiology: a laboratory manual, 11th edn. Pearson Education Ltd, London, p 561
Cheng C, Wang Q, He LY, Huang Z, Sheng XF (2015) Chitinophaga qingshengii sp. nov., isolated from weathered rock surface. Int J Syst Evol Microbiol 65:280–285
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu X-W, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466
Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porrass- Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642
Collins CH, Lyne PM, Grange JM, Falkinham JO III (2004) Collins and Lyne’s microbiological methods, 8th edn. Arnold Publishers, London, pp 168–186
Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Nat Acad Sci USA 106:16428–16433
DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689
Denner E, Paukner S, Kämpfer P, Moore E, Abraham W-R, Busse H-J, Wanner G, Lubitz W (2001) Sphingomonas pituitosa sp. nov., an exopolysaccharide-producing bacterium that secretes an unusual type of sphingan. Int J Syst Evol Microbiol 51:827–841
Döbereiner J, Baldani VL, Reis VM (1995) Endophytic occurrence of diazotrophic bacteria in non-leguminous crops. In: Fendrik I, del Gallo M, Vanderleyden J, de Zamaroczy M (eds) Azospirillum VI and related microorganisms. Springer, New York, pp 3–14
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Gao J-l, Sun P, Wang X-M, Cheng S, Lv F, Qiu T-l, Yuan M, Sun JG (2016) Sphingomonas zeicaulis sp. nov., an endophytic bacterium isolated from maize root. Int J Syst Evol Microbiol 66:3755–3760
Glaeser SP, Kämpfer P (2014) The family Sphingomonadaceae. In: Rosenberg E, DeLong E, Lory S, Stackebrandt E, Thomspon F (eds) The prokaryotes: Alphaproteobacteria and Betaproteobacteria, 4th edn. Springer, New York, pp 641–707
Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol Plant Microbe Int 17:1078–1085
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589
Kaur V, Bera MB, Panesar PS, Kumar H, Kennedy J (2014) Welan gum: microbial production, characterization, and applications. Int J Biol Macromol 65:454–461
Kim B, Wimpenny J (1981) Growth and cellulolytic activity of Cellulomonas flavigena. Can J Microbiol 27:1260–1266
Kim H, Nishiyama M, Kunito T, Senoo K, Kawahara K, Murakami K, Oyaizu H (1998) High population of Sphingomonas species on plant surface. J Appl Microbiol 85:731–736
Kim M, Oh HS, Park SC, Chun J (2014a) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351
Kim SJ, Moon JY, Lim JM, Ahn JH, Weon HY, Ahn TY, Kwon SW (2014b) Sphingomonas aerophila sp. nov. and Sphingomonas naasensis sp. nov., isolated from air and soil, respectively. Int J Syst Evol Microbiol 64:926–932
Lee J-S, Shin YK, Yoon J-H, Takeuchi M, Pyun Y-R, Park YH (2001) Sphingomonas aquatilis sp. nov., Sphingomonas koreensis sp. nov., and Sphingomonas taejonensis sp. nov., yellow-pigmented bacteria isolated from natural mineral water. Int J Syst Evol Microbiol 51:1491–1498
Li H, Jiao X, Sun Y, Sun S, Feng Z, Zhou W, Zhu H (2016) The preparation and characterization of a novel sphingan WL from marine Sphingomonas sp. WG. Sci Rep 6:37899
Maddison WP, Maddison DR (2019) Mesquite: a modular system for evolutionary analysis. Version 3.61. http://www.mesquiteproject.org/
Madhaiyan M, Peng N, Te N, Hsin I, Lin C, Lin F, Reddy C, Yan H, Ji L (2013a) Improvement of plant growth and seed yield in Jatropha curcas by a novel nitrogen-fixing root associated Enterobacter species. Biotechnol Biofuels 6:140
Madhaiyan M, Peng N, Ji L (2013b) Complete genome sequence of Enterobacter sp. strain R4-368, an endophytic N-fixing Gammaproteobacterium isolated from surface-sterilized roots of Jatropha curcas L. Genome Announc 1:e00544-00513
Madhaiyan M, Jin TY, Roy JJ, Kim S-J, Weon H-Y, Kown SW, Ji L (2013c) Pleomorphomonas diazotrophica sp. nov., a novel endophytic N-fixing bacterium isolated from the root tissue of Jatropha curcas L. Int J Syst Evol Microbiol 63:2477–2483
Madhaiyan M, Hu CJ, Roy JJ, Kim S-J, Weon H-Y, Kwon SW, Ji L (2013d) Aureimonas jatrophae sp. nov. and Aureimonas phyllosphaerae sp. nov., leaf-associated bacteria isolated from Jatropha curcas L. Int J Syst Evol Microbiol 63:1702–1708
Madhaiyan M, Hu CJ, Kim SJ, Weon HY, Kwon SW, Ji L (2013e) Jatrophihabitans endophyticus gen. nov., sp. nov., an endophytic actinobacterium isolated from a surface-sterilized stem of Jatropha curcas L. Int J Syst Evol Microbiol 63:1241–1248
Madhaiyan M, Chan KL, Ji L (2014) Draft genome sequence of Methylobacterium sp. strain L2-4, a leaf-associated endophytic N-fixing bacterium isolated from Jatropha curcas L. Genome Announc 2:e01306–e01314
Madhaiyan M, Alex THH, Te Ngoh S, Prithiviraj B, Ji L (2015) Leaf-residing Methylobacterium species fix nitrogen and promote biomass and seed production in Jatropha curcas. Biotechnol Biofuels 8:222
Madhaiyan M, Alex THH, Cho H, Kim SJ, Weon HY, Kwon SW, Whitman WB, Ji L (2017) Sphingomonas jatrophae sp. nov. and Sphingomonas carotinifaciens sp. nov., two yellow-pigmented endophytes isolated from stem tissues of Jatropha curcas L. Int J Syst Evol Microbiol 67:5150–5158
Madhaiyan M, Saravanan VS, Blom J, Smits THM, Rezzonico F, Kim SJ, Weon H-Y, Kwon S-W, Whitman WB, Ji L (2020a) Phytobacter palmae sp. nov., a novel endophytic, N2 fixing, plant growth promoting Gammaproteobacterium isolated from oil palm (Elaeis guineensis Jacq.). Int J Syst Evol Microbiol 70:841–848
Madhaiyan M, Saravanan VS, Wirth JS, Whitman WB (2020b) Reclassification of Sphingomonas aeria as a later heterotypic synonym of Sphingomonas carotinifaciens based on whole-genome sequence analysis. Int J Syst Evol Microbiol 70:2355–2358
Manandhar P, Zhang G, Hu Y, Lama A, Gao F, Gu Z (2016) Sphingomonas prati sp. nov., isolated from alpine meadow soil. Int J Syst Evol Microbiol 66:4269–4275
Manandhar P, Zhang G, Lama A, Liu F, Hu Y (2017) Sphingomonas montana sp. nov., isolated from a soil sample form the Tanggula mountain in the Qinghai Tibetan Plateau. Antonie Van Leeuwenhoek 110:1659–1668
Markowitz VM, Mavromatis K, Ivanova NN, Chen IM, Chu K, Kyrpides NC (2009) A system for microbial genome annotation expert review and curation. Bioinformatics 25:2271–2278
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60
Minnikin D, O’donnell A, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274
Prajapati VD, Jani GK, Zala BS, Khutliwala TA (2013) An insight into the emerging exopolysaccharide gellan gum as a novel polymer. Carbohydr Polym 93:670–678
Reddy GSN, Garcia-Pichel F (2007) Sphingomonas mucosissima sp. nov. and Sphingomonas desiccabilis sp. nov., from biological soil crusts in the Colorado Plateau, USA. Int J Syst Evol Microbiol 57:1028–1034
Reinhold-Hurek B, Hurek T, Claeyssens M, Van Montagu M (1993) Cloning, expression in Escherichia coli, and characterization of cellulolytic enzymes of Azoarcus sp., a root-invading diazotroph. J Bacteriol 175:7056–7065
Reinhold-Hurek B, Maes T, Gemmer S, Von Montagu M, Hurek T (2006) An endoglucanase is involved in infection of rice roots by the not cellulose-metabolizing endophyte Azoarcus sp. strain BH72. Molec Plant Microbe Interact 19:181–188
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Nat Acad Sci USA 106:19126–19131
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. MIDI Inc, Newark
Sheu SY, Xie YR, Kwon SW, Sheu C, Chen WM (2019) Sphingomonas crocodyli sp. nov., isolated from a crocodile pond. Int J Syst Evol Microbiol 69:2153–2160
Wang Z, Zeng Q, Fang Z, Zhu D, Xu D, Wang G, Zheng S (2019) Sphingomoans aracearum sp. nov., isolated from rhizospheric soil of Araceae Plants. Int J Syst Evol Microbiol 697:2972–2978
Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) International Committee on Bacterial Systematics. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464
White DC, Sutton SD, Ringelberg DB (1996) The genus Sphingomonas: physiology and ecology. Curr Opin Biotechnol 7:301–306
Wilson K (1997) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston E, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. Wiley, New York, pp 2.4.1–2.4.5
Wirth JS, Whitman WB (2018) Phylogenomic analyses of a clade within the Roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 68:2393–2411
Yabuuchi E, Kosako Y, Fujiwara N, Naka T, Matsunaga I, Ogura H, Kobayashi K (2002) Emendation of the genus Sphingomonas. In: Yabuuchi et al. 1990 and junior objective synonymy of the species of three genera, Sphingobium, Novosphingobium and Sphingopyxis, in conjunction with Blastomonas ursincola. Int J Syst Evol Microbiol 52:1485–1496
Acknowledgements
This work was supported by the Temasek Foundation and the Singapore Economy Development Board (EDB). The genome sequencing was conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, and was supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. We also acknowledge assistance of Nikos C. Kyrpides, Tanja Woyke, Nicole Shapiro, and the other members of the JGI microbial genome sequencing team.
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MM and THHA isolated the strains, cultivated, performed electron microscopic analysis and deposited the strains, MM, JSW and VSS, constructed the 16S phylogeny and wrote the manuscript, analysed the data and prepared tables and figures, JSW MM and WBW constructed the genome based phylogeny and genome sequencing, MM, SJK, HYW and SWK have conducted the biochemical analysis, polar lipids and polyamine determination, LJ supervised the study. All authors read and approved the final version of the manuscript.
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The 16S rRNA gene sequences of the strains JS21-1T and S6-262T were deposited in GenBank/EMBL/DDBJ under the accession numbers are KX893410 and JQ660211, respectively. The draft genome sequences of the strains JS21-1T and S6-262T are available at the following accessions FNZZ00000000.1 and FOCF00000000.1, respectively.
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Madhaiyan, M., Saravanan, V.S., Wirth, J.S. et al. Sphingomonas palmae sp. nov. and Sphingomonas gellani sp. nov., endophytically associated phyllosphere bacteria isolated from economically important crop plants. Antonie van Leeuwenhoek 113, 1617–1632 (2020). https://doi.org/10.1007/s10482-020-01468-5
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DOI: https://doi.org/10.1007/s10482-020-01468-5