Abstract
Antarctic hairgrass, Deschampsia antarctica Desv. (Poaceae), is one of the two flowering plants that have an established presence in Maritime Antarctica. It has adapted to varying edaphic and climatic conditions. D. antarctica’s associations with soil-dwelling bacteria have long been suspected to add to its remarkable resilience. In this study, three compartments within D. antarctica root system and soil have been investigated as microbial habitats: the rhizosphere (root-adjacent soil particles), rhizoplane (root surface) and endosphere (root interior). For this purpose, a modification of existing methods of bacterial extraction from cryophilic plant rhizocompartments was devised with the temperature sensitivity of the source material in mind. Next-generation targeted 16S rRNA gene amplicon sequencing and a culture-based approach were employed to explore the bacterial community residing within those three rhizocompartments. Results showed that each of the compartments housed a distinct bacterial community not only in terms of phylogenetic diversity but also concerning plant-beneficial and -adaptive traits. Although most cultivable bacteria displayed plant-growth promoting abilities such as rock-phosphate solubilisation and phytohormone production (Arthrobacter spp.), some could be potential pathogens (Clavibacter sp.). This study highlights the need for amending the still scarce information on the microbiome of Antarctic flora but also gives tools and insight to explore it further.
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References
Ahmed M, Stal LJ, Hasnain S (2014) Biofilm formation and indole-3-acetic acid production by two rhizospheric unicellular cyanobacteria. J Microbiol Biotechnol 24:1015–1025. https://doi.org/10.4014/jmb.1310.10099
Ali MA, Naveed M, Mustafa A, Abbas A (2017) The good, the bad, and the ugly of rhizosphere microbiome. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics and plant health. Springer, Singapore, pp 253–290
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Atlas RM (2010) Handbook of microbiological media. CRC Press, Boca Raton
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
Bünger W, Jiang X, Müller J, Hurek T, Reinhold-Hurek B (2020) Novel cultivated endophytic Verrucomicrobia reveal deep-rooting traits of bacteria to associate with plants. Sci Rep 10:1–13. https://doi.org/10.1038/s41598-020-65277-6
Burton E, Yakandawala N, LoVetri K, Madhyastha MS (2007) A microplate spectrofluorometric assay for bacterial biofilms. J Ind Microbiol Biot 34:1–4. https://doi.org/10.1007/s10295-006-0086-3
de Scally SZ, Makhalanyane TP, Frossard A, Hogg ID, Cowan DA (2016) Antarctic microbial communities are functionally redundant, adapted and resistant to short term temperature perturbations. Soil Biol Biochem 103:160–170. https://doi.org/10.1016/j.soilbio.2016.08.013
de Serrano LO, Camper AK, Richards AM (2016) An overview of siderophores for iron acquisition in microorganisms living in the extreme. Biometals 29:551–571. https://doi.org/10.1007/s10534-016-9949-x
de Zelicourt A, Al-Yousif M, Hirt H (2013) Rhizosphere microbes as essential partners for plant stress tolerance. Mol Plant 6:242–245. https://doi.org/10.1093/mp/sst028
Domracheva LI, Shirokikh IG, Fokina AI (2010) Anti-Fusarium activity of cyanobacteria and actinomycetes in soil and rhizosphere. Microbiology 79:871–876. https://doi.org/10.1134/S0026261710060263
Doornbos RF, van Loon LC, Bakker PA (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32:227–243. https://doi.org/10.1007/s13593-011-0028-y
Dsouza M, Taylor MW, Turner SJ, Aislabie J (2015) Genomic and phenotypic insights into the ecology of Arthrobacter from Antarctic soils. BMC Genomics 16:36. https://doi.org/10.1186/s12864-015-1220-2
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. PNAS 112:E911–E920. https://doi.org/10.1073/pnas.1414592112
Eichenlaub R, Gartemann KH, Burger A (2007) Clavibacter michiganensis, a group of gram-positive phytopathogenic bacteria. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 385–421
Garcia R, Müller R (2014) The family Polyangiaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin
Gartemann KH, Kirchner O, Engemann J, Gräfen I, Eichenlaub R, Burger A (2003) Clavibacter michiganensis subsp. michiganensis: first steps in the understanding of virulence of a gram-positive phytopathogenic bacterium. J Biotechnol 106:179–191. https://doi.org/10.1016/j.jbiotec.2003.07.011
Giełwanowska I, Szczuka E, Bednara J, Górecki R (2005) Anatomical features and ultrastructure of Deschampsia antarctica (Poaceae) leaves from different growing habitats. Ann Bot 96:1109–1119. https://doi.org/10.1093/aob/mci262
Grzesiak J, Kaczyńska A, Gawor J, Żuchniewicz K, Aleksandrzak-Piekarczyk T, Gromadka R, Zdanowski MK (2020) A smelly business: microbiology of Adélie penguin guano (Point Thomas rookery, Antarctica). STOTEN 714:136714. https://doi.org/10.1016/j.scitotenv.2020.136714
Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14. https://doi.org/10.1007/s11104-007-9514-z
Hoster F, Schmitz JE, Daniel R (2005) Enrichment of chitinolytic microorganisms: isolation and characterization of a chitinase exhibiting antifungal activity against phytopathogenic fungi from a novel Streptomyces strain. Appl Microbiol Biotechnol 66:434–442. https://doi.org/10.1007/s00253-004-1664-9
Huang XF, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92:267–275. https://doi.org/10.1139/cjb-2013-0225
Jangid K, Whitman WB, Condron LM, Turner BL, Williams MA (2013) Soil bacterial community succession during long-term ecosystem development. Mol Ecol 22:3415–3424. https://doi.org/10.1111/mec.12325
Jenkins C, Staley JT (2013) History, classification and cultivation of the planctomycetes. In: Fuerst J (ed) Planctomycetes: cell structure, origins and biology. Humana Press, Totowa, NJ
Jiang Y, Wu Y, Xu W, Cheng Y, Chen J, Xu L et al (2012) IAA-producing bacteria and bacterial-feeding nematodes promote Arabidopsis thaliana root growth in natural soil. Eur J Soil Biol 52:20–26. https://doi.org/10.1016/j.ejsobi.2012.05.003
Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE (2016) The ecology of acidobacteria: moving beyond genes and genomes. Front Microbiol 7:744. https://doi.org/10.3389/fmicb.2016.00744
Kim OS, Chae N, Lim HS, Cho A, Kim JH, Hong SG, Oh J (2012) Bacterial diversity in ornithogenic soils compared to mineral soils on King George Island, Antarctica. J Microbiol 50:1081–1085. https://doi.org/10.1007/s12275-012-2655-7
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1. https://doi.org/10.1093/nar/gks808
Koeck DE, Pechtl A, Zverlov VV, Schwarz WH (2014) Genomics of cellulolytic bacteria. Curr Opin Biotechnol 29:171–183. https://doi.org/10.1016/j.copbio.2014.07.002
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
Łachacz A, Kalisz B, Giełwanowska I, Olech M, Chwedorzewska KJ, Kellmann-Sopyła W (2018) Nutrient abundance and variability from Antarctic soils in the coastal of King George Island. J Soil Sci Plant Nutr 18:294–311. https://doi.org/10.4067/S0718-95162018005001101
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chinchester, pp 115–175
Lang M, Bei S, Li X, Kuyper TW, Zhang J (2019) Rhizoplane bacteria and plant species co-determine phosphorus-mediated microbial legacy effect. Front Microbiol 10:2856. https://doi.org/10.3389/fmicb.2019.02856
Liu M, Li YH, Liu Y, Zhu JN, Liu QF, Liu Y et al (2011) Flavobacterium phragmitis sp. nov., an endophyte of reed (Phragmites australis). Int J Syst Evol Micr 61:2717–2721. https://doi.org/10.1099/ijs.0.027417-0
McBride MJ (2014) The family Flavobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin
McBride MJ, Liu W, Lu X, Zhu Y, Zhang W (2014) The family Cytophagaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin
Mosyakin SL, Bezusko LG, Mosyakin AS (2007) Origins of native vascular plants of Antarctica: comments from a historical phytogeography viewpoint. Cytol Genet 41:308–316. https://doi.org/10.3103/S009545270705009X
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
Newsham KK, Tripathi BM, Dong K, Yamamoto N, Adams JM, Hopkins DW (2019) Bacterial community composition and diversity respond to nutrient amendment but not warming in a maritime Antarctic soil. Microb Ecol 78:974–984. https://doi.org/10.1007/s00248-019-01373-z
Olave-Concha N, Bravo LA, Ruiz-Lara S, Corcuera LJ (2005) Differential accumulation of dehydrin-like proteins by abiotic stresses in Deschampsia antarctica Desv. Polar Biol 28:506–513. https://doi.org/10.1007/s00300-005-0718-5
Park JS, Ahn IY, Lee EJ (2012) Influence of soil properties on the distribution of Deschampsia antarctica on King George Island, Maritime Antarctica. Polar Biol 35:1703–1711. https://doi.org/10.1657/1938-4246-45.4.563
Reasoner DJ, Geldreich EE (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49:1–7. https://doi.org/10.1128/aem.49.1.1-7.1985
Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF et al (2002) A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (Lf) Druce. Appl Environ Microbiol 68:5217–5222. https://doi.org/10.1128/AEM.68.11.5217-5222.2002
Rodrigues AA, Forzani MV, Soares RDS, Sibov ST, Vieira JDG (2016) Isolation and selection of plant growth-promoting bacteria associated with sugarcane. Pesqui Agropecu Trop 46:149–158. https://doi.org/10.1590/1983-40632016v4639526
Romaniuk K, Ciok A, Decewicz P, Uhrynowski W, Budzik K, Nieckarz M, Dziewit L (2018) Insight into heavy metal resistome of soil psychrotolerant bacteria originating from King George Island (Antarctica). Polar Biol 41:1319–1333. https://doi.org/10.1007/s00300-018-2287-4
Rosenberg E (2014) The phylum fibrobacteres. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin
Ruhland CT, Krna MA (2010) Effects of salinity and temperature on Deschampsia antarctica. Polar Biol 33:1007–1012. https://doi.org/10.1017/S0954102016000249
Saha R, Saha N, Donofrio RS, Bestervelt LL (2013) Microbial siderophores: a mini review. J Basic Microbiol 53:303–317. https://doi.org/10.1002/jobm.201100552
Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41. https://doi.org/10.1016/j.tplants.2017.09.003
Teixeira LC, Peixoto RS, Cury JC, Sul WJ, Pellizari VH, Tiedje J, Rosado AS (2010) Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME 4:989–1001. https://doi.org/10.1002/9781118297674.ch105
Tistechok S, Skvortsova M, Luzhetskyy A, Fedorenko V, Parnikoza I, Gromyko O (2019) Antagonistic and plant growth promoting properties of actinomycetes from rhizosphere Deschampsia antarctica È. Desv. (Galindez Island, Antarctica). UAJ 1:169–177
Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:1–10. https://doi.org/10.1186/gb-2013-14-6-209
Tytgat B, Verleyen E, Sweetlove M, Dhondt S, Clercx P, Van Ranst E et al (2016) Bacterial community composition in relation to bedrock type and macrobiota in soils from the Sør Rondane Mountains. East Antarctica. FEMS Microbiol Ecol 92:fiw126. https://doi.org/10.1093/femsec/fiw126
van der Heijden MG, Schlaeppi K (2015) Root surface as a frontier for plant microbiome research. PNAS 112:2299–2300. https://doi.org/10.1073/pnas.1500709112
Velji MI, Albright LJ (1986) Microscopic enumeration of attached marine bacteria of seawater, marine sediment, fecal matter, and kelp blade samples following pyrophosphate and ultrasound treatments. Can J Microbiol 32:121–126. https://doi.org/10.1139/m86-024
Wang NF, Zhang T, Zhang F, Wang ET, He JF, Ding H et al (2015) Diversity and structure of soil bacterial communities in the Fildes Region (maritime Antarctica) as revealed by 454 pyrosequencing. Front Microbiol 6:1188. https://doi.org/10.3389/fmicb.2015.01188
Weidner S, Arnold W, Puhler A (1996) Diversity of uncultured microorganisms associated with the seagrass Halophila stipulacea estimated by restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol 62:766–771. https://doi.org/10.1128/aem.62.3.766-771.1996
Wingett SW, Andrews S (2018) FastQ Screen: a tool for multi-genome mapping and quality control. F1000Res 24:1338
Wu L, Chen J, Xiao Z, Zhu X, Wang J, Wu H et al (2018) Barcoded pyrosequencing reveals a shift in the bacterial community in the rhizosphere and rhizoplane of Rehmannia glutinosa under consecutive monoculture. Int Journal Mol Sci 19:850. https://doi.org/10.3390/ijms19030850
Yang L, Liu Y, Wu H, Høiby N, Molin S, Song ZJ (2011) Current understanding of multi-species biofilms. Int J Oral Sci 3:74–81. https://doi.org/10.4248/ijos11027
Yoon WB, Rosson RA (1990) Improved method of enumeration of attached bacteria for study of fluctuation in the abundance of attached and free-living bacteria in response to diel variation in seawater turbidity. App Environ Microbiol 56:595–600. https://doi.org/10.1128/aem.56.3.595-600.1990
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613. https://doi.org/10.1099/ijsem.0.001755
Yu X, Zhang W, Lang D, Zhang X, Cui G, Zhang X (2019) Interactions between endophytes and plants: beneficial effect of endophytes to ameliorate biotic and abiotic stresses in plants. J Plant Biol 62:1–13. https://doi.org/10.1007/s12374-018-0274-5
Yudakova OI, Tyrnov VS, Kunakh VA, Kozeretskaya IA, Parnikoza IY (2016) Adaptation of the seed reproduction system to conditions of Maritime Antarctic in Deschampsia antarctica E. Desv Russ J Dev Biol 47:138–146. https://doi.org/10.1134/S1062360416030073
Zdanowski MK, Żmuda-Baranowska MJ, Borsuk P, Świątecki A, Górniak D, Wolicka D, Grzesiak J (2013) Culturable bacteria community development in postglacial soils of Ecology Glacier, King George Island, Antarctica. Polar Biol 36:511–527. https://doi.org/10.1007/s00300-012-1278-0
Znój A, Chwedorzewska KJ, Androsiuk P, Cuba-Diaz M, Giełwanowska I, Koc J, Korczak-Abshire M, Grzesiak J, Zmarz A (2017) Rapid environmental changes in the Western Antarctic Peninsula region due to climate change and human activity. Appl Ecol Environ Res 15:525–539
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Samples and data were obtained using the scientific facility of the “H. Arctowski” Polish Antarctic Station. We are very grateful to Carla Caruso and Leticia Barrientos for the review of this paper and insightful comments.
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This work was supported by the National Science Center, Poland (Grant 2016/21/N/NZ9/01536).
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Study design: JG; experiment performance: AZ, JG; data analysis: JG; manuscript preparation: JG; manuscript edition: AZ, JG, RG, KJC.
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Znój, A., Grzesiak, J., Gawor, J. et al. Highly specialized bacterial communities within three distinct rhizocompartments of Antarctic hairgrass (Deschampsia antarctica Desv.). Polar Biol 45, 833–844 (2022). https://doi.org/10.1007/s00300-022-03027-2
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DOI: https://doi.org/10.1007/s00300-022-03027-2