Abstract
In association with lichens, bacteria can play key roles in solubilizing sources of inorganic phosphates that are available in the environment. In this study, the potential of bacteria isolated from 15 Antarctic lichen samples for phosphate solubilization was investigated. From 124 bacteria tested, 66 (53%) were positive for phosphate solubilization in solid NBRIP medium, with a higher prevalence of Pseudomonas, followed by Caballeronia and Chryseobacterium. Most of the phosphate-solubilizing bacteria were isolated from Usnea auratiacoatra, followed by Caloplaca regalis and Xanthoria candelaria. Two isolates showed outstanding performance, Pseudomonas sp. 11.LB15 and Pseudomonas sp. 1.LB34, since they presented solubilization in the temperature range from 15.0 to 30.0 °C, and maximum quantification of soluble phosphate at 25.0 °C was 511.21 and 532.07 mg/L for Pseudomonas sp. 11.LB15 and Pseudomonas sp. 1.LB34, respectively. At 30.0 °C soluble phosphate yield was 639.43 and 518.95 mg/L with pH of 3.74 and 3.87 for Pseudomonas sp. 11.LB15 and Pseudomonas sp. 1.LB34, respectively. Fumaric and tartaric acids were released during the solubilization process. Finally, bacteria isolated from Antarctic lichens were shown to have the potential for phosphate solubilization, opening perspectives for future application in the agricultural sector and contributing to reduce the use of chemical fertilizers.
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References
Almeida JMGCF (2005) Yeast community survey in the Tagus estuary. FEMS Microbiol Ecolo 53:295–303. https://doi.org/10.1016/j.femsec.2005.01.006
Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol 8:971. https://doi.org/10.3389/fmicb.2017.00971
Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555. https://doi.org/10.1016/j.mimet.2003.08.009
Barrientos-Díaz L, Gidekel M, Gutiérrez-Moraga A (2008) Characterization of rhizospheric bacteria isolated from Deschampsia antarctica Desv. World J Microbiol Biotechnol 24:2289. https://doi.org/10.1007/s11274-008-9743-1
Benavent-González A, Delgado-Baquerizo M, Fernández-Brun L, Singh BK, Maestre FT, Sancho LG (2018) Identity of plant, lichen and moss species connects with microbial abundance and soil functioning in maritime Antarctica. Plant Soil 429:35–52. https://doi.org/10.1007/s11104-018-3721-7
Berríos G, Cabrera G, Gidekel M, Gutiérrez-Moraga A (2013) Characterization of a novel Antarctic plant growth-promoting bacterial strain and its interaction with Antarctic hair grass (Deschampsia antarctica Desv). Polar Biol 36:349–362. https://doi.org/10.1007/s00300-012-1264-6
Cernava T, Erlacher A, Aschenbrenner IA, Krug L, Lassek C, Riedel K, Grube M, Berg G (2017) Deciphering functional diversification within the lichen microbiota by meta-omics. Microbiome 5:82. https://doi.org/10.1186/s40168-017-0303-5
Cernava T, Aschenbrenner IA, Soh J, Sensen CW, Grube M, Berg G (2019) Plasticity of a holobiont: desiccation induces fasting-like metabolism within the lichen microbiota. ISME J 13:547–556. https://doi.org/10.1038/s41396-018-0286-7
Cherchali A, Boukhelata N, Kaci Y, Abrous-Belbachir O, Djebbar R (2019) Isolation and identification of a phosphate-solubilizing Paenibacillus polymyxa strain GOL 0202 from durum wheat (Triticum durum Desf.) rhizosphere and its effect on some seedlings morphophysiological parameters. Biocatal Agric Biotechnol 19:101087. https://doi.org/10.1016/j.bcab.2019.101087
Duarte AWF, Passarini MRZ, Delforno TP, Pellizzari FM, Cipro CVZ, Montone RC, Petry MV, Putzke J, Rosa LH, Sette LD (2016) Yeasts from macroalgae and lichens that inhabit the South Shetland Islands, Antarctica. Environ Microbiol 8:874–885. https://doi.org/10.1111/1758-2229.12452
Gaur AC (1990) Phosphate solubilizing microorganisms as biofertilizers. Omega Scientific Publication, New Delhi, Almora, Uttarakhand
Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C, Wegner U, Becher D, Riedel K, Sensen CW, Berg G (2015) Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J 9:412–424. https://doi.org/10.1038/ismej.2014.138
Gulati A, Rahi P, Vyas P (2008) Characterization of phosphate-solubilizing fluorescent pseudomonads from the rhizosphere of seabuckthorn growing in the cold deserts of Himalayas. Curr Microbiol 56:73. https://doi.org/10.1007/s00284-007-9042-3
Gupta P, Kumar V (2016) Value added phytoremediation of metal stressed soils using phosphate solubilizing microbial consortium. World J Microbiol Biotechnol 33:9. https://doi.org/10.1007/s11274-016-2176-3
Gyaneshwar P, Parekh LJ, Archana G, Poole PS, Collins MD, Hutson RA, Kumar GN (1999) Involvement of a phosphate starvation inducible glucose dehydrogenase in soil phosphate solubilization by Enterobacter asburiae. FEMS Microbiol Lett 171:223–229. https://doi.org/10.1111/j.1574-6968.1999.tb13436.x
Hamdali H, Bouizgarne B, Hafidi M, Lebrihi A, Virolle MJ, Ouhdouch Y (2008) Screening for rock phosphate solubilizing Actinomycetes from Moroccan phosphate mines. Appl Soil Ecolo 38:12–19. https://doi.org/10.1016/j.apsoil.2007.08.007
Hawksworth DL, Grube M (2020) Lichens redefined as complex ecosystems. New Phytol 227:1281–1283. https://doi.org/10.1111/nph.16630
Hii YS, San CY, Lau SW, Danquah MK (2020) Isolation and characterisation of phosphate solubilizing microorganisms from peat. Biocatal Agric Biotechnol 26:101643. https://doi.org/10.1016/j.bcab.2020.101643
Jha A, Saxena J, Sharma V (2013) Investigation on phosphate solubilization potential of agricultural soil bacteria as affected by different phosphorus sources, temperature, salt and pH. Commun Soil Sci Plant Anal 44:2443–2458. https://doi.org/10.1080/00103624.2013.803557
Kang SC, Ha GC, Lee TG, Maheshwari DK (2002) Solubilization of insoluble inorganic phosphates by a soil inhabiting fungus sp. Ps 102. Curr Sci 79:439–442
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Li L, Chen R, Zuo Z, Lv Z, Yang Z, Mao W, Liu Y, Zhou Y, Huang J, Song Z (2020) Evaluation and improvement of phosphate solubilization by an isolated bacterium Pantoea agglomerans ZB. World J Microbiol Biotechnol 36:27. https://doi.org/10.1007/s11274-019-2744-4
Matsuoka K, Skoglund A, Roth G (2018) Quantarctica. Nor Polar Inst. https://doi.org/10.2134/npolar.2018.8516e961
Naruya S, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
Noh HJ, Baek K, Hwang CY, Shin SC, Hong SG, Lee YM (2019) Lichenihabitans psoromatis gen. nov., sp. nov., a member of a novel lineage (Lichenihabitantaceae fam. nov.) within the order of Rhizobiales isolated from Antarctic lichen. Int J Syst Evol Micr 69:3837–3842. https://doi.org/10.1099/ijsem.0.003695
O’Halloran IP, Cade-Menun BJ (2006) Total and organic phosphorus. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis. CRC Press, Boca Raton, pp 265–291
Palmqvist K, Dahlman L, Jonsson A, Nash TH (2008) The carbon economy of lichens. In: Nash TH (ed) Lichen biology. Cambridge University Press, New York, pp 182–215
Pandey A, Yarzábal LA (2019) Bioprospecting cold-adapted plant growth promoting microorganisms from mountain environments. Appl Microbiol Biotechnol 103:643–657. https://doi.org/10.1007/s00253-018-9515-2
Park KH, Lee CY, Son HJ (2009) Mechanism of insoluble phosphate solubilization by Pseudomonas fluorescens RAF15 isolated from ginseng rhizosphere and its plant growth-promoting activities. Lett Appl Microbiol 49:222–228. https://doi.org/10.1111/j.1472-765X.2009.02642.x
Puvar AC, Nathani NM, Shaikha I, Bhatt AD, Bhargava P, Joshi CG, Joshi MN (2020) Bacterial line of defense in Dirinaria lichen from two different ecosystems: first genomic insights of its mycobiont Dirinaria sp. GBRC AP01. Microbiol Res. 233:126407. https://doi.org/10.1016/j.micres.2019.126407
Rasul M, Yasmin S, Zubair M, Mahreen N, Yousaf S, Arif M, Sajid ZI, Mirza MS (2019) Phosphate solubilizers as antagonists for bacterial leaf blight with improved rice growth in phosphorus deficit soil. Biol Control. https://doi.org/10.1016/j.biocontrol.2019.05.016
Sampaio JP, Gadanho M, Santos S, Duarte FL, Pais C, Fonseca A, Fell JW (2001) Polyphasic taxonomy of the basidiomycetous yeast genus Rhodosporidium: Rhodosporidium kratochvilovae and related anamorphic species. Int J Syst Evol Micr 51:687–697. https://doi.org/10.1099/00207713-51-2-687
Sang MK, Jeong JJ, Kim J, Kim KD (2018) Growth promotion and root colonisation in pepper plants by phosphate-solubilising Chryseobacterium sp. strain ISE14 that suppresses Phytophthora blight. Ann Appl Biol 172:208–223. https://doi.org/10.1111/aab.12413
Santiago IF, Soares MA, Rosa CA, Rosa LH (2015) Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles 19:1087–1097. https://doi.org/10.1007/s00792-015-0781-y
Sarikhani MR, Khoshru B, Greiner R (2019) Isolation and identification of temperature tolerant phosphate solubilizing bacteria as a potential microbial fertilizer. World J Microbiol Biotechnol 35:126. https://doi.org/10.1007/s11274-019-2702-1
Schmitz D, Putzke J, Albuquerque MP, Schünemann AL, Vieira FCB, Victoria FC, Pereira AB (2018) Description of plant communities on Half Moon Island Antarctica. Polar Res 37:1. https://doi.org/10.1080/17518369.2018.1523663
Sigurbjörnsdóttir MA, Vilhelmsson O (2016) Selective isolation of potentially phosphate-mobilizing, biosurfactant-producing and biodegradative bacteria associated with a sub-Arctic, terricolous lichen, Peltigera membranacea. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiw090
Sigurbjörnsdóttir MA, Heiðmarsson S, Jónsdóttir AR, Vilhelmsson O (2014) Novel bacteria associated with Arctic seashore lichens have potential roles in nutrient scavenging. Can J Microbiol 60:307–317. https://doi.org/10.1139/cjm-2013-0888
Singh SM, Olech M, Cannone N, Convey P (2015) Contrasting patterns in lichen diversity in the continental and maritime Antarctic. Polar Sci 9:311–318. https://doi.org/10.1016/j.polar.2015.07.001
Stevenson FJ, Cole MA (1999) Cycles of soils: carbon, nitrogen, phosphorus, sulfur, micronutrients. Wiley, New York
Teodosieva R, Bojinova D (2016) Biodecomposition of Jordan phosphorite by phosphate-solubilizing Fungi. Braz J Chem Eng 33:1–11. https://doi.org/10.1590/0104-6632.20160331s00003267
Tuovinen V, Ekman S, Thor G, Vanderpool D, Spribille T, Johannesson H (2019) Two basidiomycete fungi in the cortex of wolf lichens. Curr Biol 29:476–483. https://doi.org/10.1016/j.cub.2018.12.022
Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing Pseudomonas fluorescent. BMC Microbiol 9:174. https://doi.org/10.1186/1471-2180-9-174
Vyas P, Rahi P, Gulati A (2009) Stress tolerance and genetic variability of phosphate-solubilizing fluorescent pseudomonas from the cold deserts of the Trans-Himalayas. Microb Ecol 58:425–434. https://doi.org/10.1007/s00248-009-9511-2
Xiang WL, Liang HZ, Liu S, Luo F, Tang J, Li MY, Che ZM (2011) Isolation and performance evaluation of halotolerant phosphate solubilizing bacteria from the rhizospheric soils of historic Dagong Brine Well in China. World J Microbiol Biotechnol 27:2629–2637. https://doi.org/10.1007/s11274-011-0736-0
Yarzábal LA, Monserrate L, Buela L, Chica E (2018) Antarctic Pseudomonas spp. promote wheat germination and growth at low temperatures. Polar Biol 41:2343–2354. https://doi.org/10.1007/s00300-018-2374-6
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The authors acknowledge the financial support from Fundação de Amparo à Pesquisa do Estado de Alagoas—FAPEAL (60030 1074/2016) and CNPq (433388/2018-8 and 442258/2018-6). A master's scholarship the first author was supported by FAPEAL (60030 000542/2018).
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da Silva, A.V., de Oliveira, A.J., Tanabe, I.S.B. et al. Antarctic lichens as a source of phosphate-solubilizing bacteria. Extremophiles 25, 181–191 (2021). https://doi.org/10.1007/s00792-021-01220-5
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DOI: https://doi.org/10.1007/s00792-021-01220-5