Abstract
A novel actinobacterium, designated strain JXJ CY 21T, was isolated from the culture mass of Microcystis sp. FACHB-905 collected from Lake Dianchi, South-west China. Polyphasic taxonomic study revealed that the isolate should be a member of the genus Citricoccus. Comparison of the 16S rRNA gene sequence of strain JXJ CY 21T with the available sequences in the GenBank database showed that the strain is closely related to Citricoccus zhacaiensis FS24T (97.8 % similarity), Citricoccus parietis 02-Je-010T (97.7 %), Citricoccus terreus V3M1T (97.6 %), Citricoccus nitrophenolicus PNP1T (97.2 %), Citricoccus alkalitolerans YIM 70010T (97.2 %) and Citricoccus muralis 4-0T (97.0 %). The DNA–DNA hybridization values between strain JXJ CY 21T and the related type strains C. zhacaiensis FS24T and C. parietis 02-Je-010T were 16.0 ± 2.6 and 5.4 ± 1.7 %, respectively. The peptidoglycan in the cell wall was A4α type containing lysine–glutamic acid–glycine. The major respiratory menaquinone was found to be MK-8 (H2) (98.5 %), while the major cellular fatty acids (>10 %) were anteiso-C15:0, iso-C16:0, iso-C15:0 and iso-C14:0. The polar lipids detected were diphosphatidylglycerol, phosphatidylinositol, phosphatidylglycerol, an unidentified phospholipid and an unidentified glycolipid. The DNA G + C content was determined to be 62.7 mol%. Strain JXJ CY 21T can solubilize both insoluble inorganic and organic phosphates up to 24.7 and 1.7 mg/l respectively. This property of the novel actinobacterium acts as a modulator for enhancement of growth of Microcystis sp. FACHB-905 in the lake ecosystem where the amount of soluble phosphate is limited. On the basis of the above taxonomic data, strain JXJ CY 21T represents a novel species of the genus Citricoccus, for which the name Citricoccus lacusdiani sp. nov. is proposed. The type strain is JXJ CY 21T (=KCTC 29653T = DSM 29160T).
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References
Altenburger P, Kämpfer P, Schumann P, Steiner R, Lubitz W, Busse HJ (2002) Citricoccus muralis gen. nov., sp. nov., a novel actinobacterium isolated from a medieval wall painting. Int J Syst Evol Microbiol 52:2095–2100
Casamatta D, Wickstrom C (2000) Sensitivity of two distinct bacterioplankton communities to exudates from the cyanobacterium Microcystis aeruginosa. Microb Ecol 41:64–73
Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41
Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Ann Rev Ecol Syst 13:291–314
Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycan based on 2, 4-diaminobutyric acid. Appl Bacteriol 48:459–470
Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230
de-Bashan LE, Antoun H, Bashan Y (2008) Involvement of indole-3-acetic-acid produced by the growth-promoting bacterium Azospirillum spp. in promoting growth of Chlorella vulgaris. J Phycol 44:938–947
Deng J, Li JH, Guan ZL, Hu BY, Zhao L, Li PF (2012) Effect of attached bacteria of carbonic anhydrase on the growth of Microcystis aeruginosa. J Lake Sci 24:429–435
Dziallas C, Grossart HP (2011) Temperature and biotic factors influence bacterial communities associated with the cyanobacterium Microcystis sp. Environ Microbiol 13:1632–1641
Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid–deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416
Goodfellow M (1971) Numerical taxonomy of some nocardioform bacteria. J Gen Microbiol 69:33–80
Hasegawa T, Takizaea M, Tanida S (1983) A rapid analysis for chemical grouping aerobic actinomycetes. J Gen Appl Microbiol 29:319–322
Jürgens K, Güde H (1994) The potential importance of grazing-resistant bacteria in planktonic systems. Mar Ecol Prog Ser 112:169–188
Kovacs N (1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178:703–704
Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 5:2359–2387
Li WJ, Chen HH, Zhang YQ, Kim CJ, Park GJ, Lee JC, Xu LH, Jiang CL (2005) Citricoccus alkalitolerans sp. nov., a novel actinobacterium isolated from a desert soil in Egypt. Int J Syst Evol Microbiol 55:87–90
Liu YM, Chen W, Li DH, Shen YW, Liu YD, Song LR (2006) Analysis of paralytic shellfish toxins in Aphanizomenon DC-1 from Lake Dianchi, China. Environ Toxicol 21:289–295
Madhaiyan M, Poonguzhali S, Lee JS, Lee KC, Saravanan VS, Santhanakrishnan P (2010) Microbacterium azadirachtae sp. nov., a plantgrowth-promoting actinobacterium isolated from the rhizoplane of neem seedlings. Int J Syst Evol Micr 60:1687–1692
Matsui T, Semba H, Hanada S (2012) Citricoccus yambaruensis sp. nov., a racemic phenylsuccinate stereospecifically assimilating actinomycete isolated from soil in Okinawa. J Gen Appl Microbiol 58:373–378
Meng FX, Yang XC, Yu PS, Pan JM, Wang CS, Xu XW, Wu M (2010) Citricoccus zhacaiensis sp. nov., isolated from a bioreactor for saline wastewater treatment. Int J Syst Evol Microbiol 60:495–499
Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G + C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39:159–167
Ministry of Agriculture of the People’s Republic of China (NY/T 1847—2010). General technical requirements for production strain quality of microbial fertilizer
Minnikin DE, Collins MD, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95
Nielsen MB, Kjeldsen KU, Ingvorsen K (2011) Description of Citricoccus nitrophenolicus sp. nov., a para-nitrophenol degrading actinobacterium isolated from a wastewater treatment plant and emended description of the genus Citricoccus Altenburger et al 2002. Antonie Van Leeuwenhoek 99(3):489–499
Niu Y, Shen H, Chen J, Xie P, Yang X, Tao M, Ma ZM, Qi M (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu. Water Res 45:4169–4182
Pan G, Zhang MM, Chen H, Zou H, Yan H (2006) Removal of cyanobacterial blooms in Taihu Lake using local soils. I. Equilibrium and kinetic screening on the flocculation of Microcystis aeruginosa using commercially soluble clays and minerals. Environ Pollut 141:195–200
Parveen B, Ravet V, Djediat C, Mary I, Quiblier C, Debroas D, Humbert JF (2013) Bacterial communities associated with Microcystis colonies differ from free-living communities living in the same ecosystem. Environ Microbiol Rep 5:716–724
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sasser M (2001) Identification of bacteria by gas chromatography of cellular fatty acids. http://www.microbialid.com/PDF/TechNote_101.pdf
Schäfer J, Martin K, Kämpfer P (2010) Citricoccus parietis sp. nov., isolated from a mould-colonized wall and emended description of Citricoccus alkalitolerans Li et al 2005. Int J Syst Evol Microbiol 60(2):271–274
Shi LM, Cai YF, Yang HL, Xing P, Li PF, Kong LD, Kong FX (2009) Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. J Environ Sci 21:1581–1590
Shi LM, Cai YF, Kong FX, Yu Y (2012) Specific association between bacteria and buoyant Microcystis colonies compared with other bulk bacterial communities in the eutrophic Lake Taihu. Env Microbiol Rep 4:669–678
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tang SK, Wang Y, Chen Y, Lou K, Cao LL, Xu LH, Li WJ (2009) Zhihengliuella alba sp. nov., and emended description of the genus Zhihengliuella. Int J Syst Evol Microbiol 59:2025–2032
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464
Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA, Sackin MJ (1983) Numerical classification of Streptomyces and related genera. J Gen Microbiol 129:1743–1813
Xu P, Li WJ, Tang SK, Zhang YQ, Chen GZ, Chen HH, Xu H, Jiang CL (2005) Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family Oxalobacteraceae isolated from China. Int J Syst Evol Microbiol 55:1149–1153
Yang LY, Xiao L (2010) Outbrust, jeopardize and control of cyanobacterial bloom in lakes. Science, Beijing, p 212
Zhang BH, Chen W, Li HQ, Hozzein WN, Yang Y, Hu WY, Abusaud O, Gao R, Li WJ (2015) A cyanobacteria-lytic compound produced by Streptomyces jiujiangensis JXJ 0074T. Appl Microbiol Biotechnol 99:7673–7683
Zhao GY, Du JJ, Jia Y, Lv YN, Han GM, Tian XJ (2012) The importance of bacteria in promoting algal growth in eutrophic lakes with limited soluble phosphorus. Ecol Eng 42:107–111
Acknowledgments
We are grateful to Prof. Yu-Guang Zhou (CGMCC, China) and Dr. Rüediger Pukall (DSMZ, Germany) for kindly providing the reference type strains. This research was supported by Natural Science Foundation of China (No. 31060010) and Environmental Conservation Department of Jiangxi Province of China (No. JXHBKJ2013-14) and Program of Jiujiang University (No. 201511). W-J Li was also supported by Guangdong Province Higher Vocational Colleges & Schools Pearl River Scholar Funded Scheme (2014).
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Zhang, BH., Salam, N., Cheng, J. et al. Citricoccus lacusdiani sp. nov., an actinobacterium promoting Microcystis growth with limited soluble phosphorus. Antonie van Leeuwenhoek 109, 1457–1465 (2016). https://doi.org/10.1007/s10482-016-0745-y
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DOI: https://doi.org/10.1007/s10482-016-0745-y