Microbiomes of Antarctic pearlwort (Colobanthus quitensis) of the maritime Antarctic: distinct diversity and core microbes in rhizosphere and endosphere compartments of the plant
- 16S rRNA gene,
- Antarctic pearlwort,
- endophytes,
- rhizosphere
Copyright (c) 2022 Ukrainian Antarctic Journal
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Abstract
Plant microbiome plays a crucial role in the plants’ performance and fitness to the environment. The latter is especially significant for the plants withstanding the unfavorable conditions of the Antarctic. The study aimed to evaluate the microbiome of Antarctic pearlwort Colobanthus quitensis (Kunth) Bartl. growing in the wide range from the South Shetland Islands in the North to Marguerite Bay in the South (63°S – 68°S) in the maritime Antarctic. The composition of C. quitensis microbiome (rhizosphere and endophytes of the plant's aerial part) was studied by 16S rRNA amplicon metagenomic sequencing on Illumina Novaseq 6000. The number of operational taxonomic units and diversity indices (Shannon, Simpson, Faith PD) of the endosphere microbiomes were lower (p < 0.05) than in the rhizosphere microbiomes, and the ANOSIM test revealed a difference (R = 0.9, p = 0.0001) in the microbiomes’ taxonomic structure. The diversity of the barren’s microbiome was lower compared to the rhizospheres’. Proteobacteria, Acidobacteria, Actinobacteria, Bacteroidota, Chloroflexi, and Verrucomicrobia were dominant in the rhizosphere. Similar phyla were found in the barren, yet the ratio of Actinobacteria was higher. Proteobacteria dominated in the endosphere, followed by Firmicutes, Actinobacteria, and Bacteroidota. Alphaproteobacteria, Actinobacteria, and Acidobacteria represented a large proportion of the core microbiota of C. quitensis rhizosphere. The endophyte microbiome’s core was mainly composed of Alphaproteobacteria, Gammaproteobacteria, and Firmicutes. On the family taxonomic level, Rhodobacteraceae, Microbacteriaceae, Rhizobiaceae, Xanthobacteraceae, Sphingomonadaceae, Comamonadaceae, Pseudomonadaceae, and Oxalobacteraceae were determined as the core for rhizosphere and endosphere. The correlation was low (R = 0.22, p = 0.04)
between the rhizosphere microbiome composition and the latitude. Nevertheless, differential abundance of some bacterial taxa in the rhizosphere was attributed to the region of the plant’s growth: Northern, Central, or Southern part of the maritime Antarctic. The shift in the composition of microbial communities can be associated with the changing of the climatic conditions southwards along the Western coast of the Antarctic Peninsula.
References
- Arocha-Garza, H. F., Canales-Del Castillo, R., Eguiarte, L. E., Souza, V., & De la Torre-Zavala, S. (2017). High diversity and suggested endemicity of culturable Actinobacteria in an extremely oligotrophic desert oasis. PeerJ, 5, e3247. https://doi.org/10.7717/peerj.3247
- Baldani, J. I., Reis, V. M., Videira, S. S., Boddey, L. H., & Baldani, V. L. D. (2014). The art of isolating nitrogen-fixing bacteria from non-leguminous plants using N-free semi-solid media: a practical guide for microbiologists. Plant and Soil, 384, 413–431. https://doi.org/10.1007/s11104-014-2186-6
- Barra, P. J., Inostroza, N. G., Acuña, J. J., Mora, M. L., Crowley, D. E., & Jorquera, M. A. (2016). Formulation of bacterial consortia from avocado (Persea americana Mill.) and their effect on growth, biomass and superoxide dismutase activity of wheat seedlings under salt stress. Applied Soil Ecology, 102, 80–91. https://doi.org/10.1016/j.apsoil.2016.02.014
- Barrientos-Díaz, L., Gidekel, M., & Gutiérrez-Moraga, A. (2008). Characterization of rhizospheric bacteria isolated from Deschampsia antarctica Desv. World Journal of Microbiology and Biotechnology, 24, 2289–2296. https://doi.org/10.1007/s11274-008-9743-1
- Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289–300.
- Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends in Plant Science, 17(8), 478–486. https://doi.org/10.1016/j.tplants.2012.04.001
- Berríos, G., Cabrera, G., Gidekel, M., & Gutiérrez-Moraga, A. (2013). Characterization of a novel Antarctic plant growthpromoting bacterial strain and its interaction with Antarctic hair grass (Deschampsia antarctica Desv). Polar Biology, 36, 349–362. https://doi.org/10.1007/s00300-012-1264-6
- Bredow, C., Azevedo, J. L., Pamphile, J. A., Mangolin, C. A., & Rhoden, S. A. (2015). In silico analysis of the 16S rRNA gene of endophytic bacteria, isolated from the aerial parts and seeds of important agricultural crops. Genetics and Molecular Research: GMR, 14(3), 9703–9721. https://doi.org/10.4238/2015.August.19.3
- Chauhan, A., Guleria, S., Balgir, P. P., Walia, A., Mahajan, R., Mehta, P., & Shirkot, C. K. (2017). Tricalcium phosphate solubilization and nitrogen fixation by newly isolated Aneurinibacillus aneurinilyticus CKMV1 from rhizosphere of Valeriana jatamansi and its growth promotional effect. Brazilian Journal of Microbiology, 48(2), 294–304. https://doi.org/10.1016/j.bjm.2016.12.001
- Chung, E. J., Park, T. S., Jeon, C. O., & Chung, Y. R. (2012). Chitinophaga oryziterrae sp. nov., isolated from the rhizosphere soil of rice (Oryza sativa L.). International Journal of Systematic and Evolutionary Microbiology, 62(Pt_12), 3030–3035. https://doi.org/10.1099/ijs.0.036442-0
- Cid, F. P., Inostroza, N. G., Graether, S. P., Bravo, L. A., & Jorquera, M. A. (2017). Bacterial community structures and ice recrystallization inhibition activity of bacteria isolated from the phyllosphere of the Antarctic vascular plant Deschampsia antarctica. Polar Biology, 40, 1319–1331. https://doi.org/10.1007/s00300-016-2036-5
- Convey, P., Hopkins, D. W., Roberts, S. J., & Tyler, A. N. (2011). Global southern limit of flowering plants and moss peat accumulation. Polar Research, 30, 8929. https://doi.org/10.3402/polar.v30i0.8929
- Convey, P., Chown, S. L., Clarke, A., Barnes, D. K. A., Bokhorst, S., Cummings, V., Ducklow, H. W., Frati, F., Green, T. G. A., Gordon, S., Griffiths, H. J., Howard-Williams, C., Huiskes, A. H. L., Laybourn-Parry, J., Lyons, W. B., McMinn, A., Morley, S. A., Peck, L. S., Quesada, A., … & Wall, D. H. (2014). The spatial structure of Antarctic biodiversity. Ecological Monographs, 84(2), 203–244. https://doi.org/10.1890/12-2216.1
- Delgado-Baquerizo, M., Oliverio, A. M., Brewer, T. E., Benavent-González, A., Eldridge, D. J., Bardgett, R. D., Maestre, F. T., Singh, B. K., & Fierer, N. (2018). A global atlas of the dominant bacteria found in soil. Science, 359(6373), 320–325. https://doi.org/10.1126/science.aap9516
- DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., & Andersen, G. L. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72(7), 5069–5072. https://doi.org/10.1128/AEM.03006-05
- Devi, K. A., Pandey, G., Rawat, A. K. S., Sharma, G. D., & Pandey, P. (2017). The Endophytic symbiont – Pseudomonas aeruginosa stimulates the antioxidant activity and growth of Achyranthes aspera L. Frontiers in Microbiology, 8, 1897. https://doi.org/10.3389/fmicb.2017.01897
- Fierer, N., Bradford, M. A., & Jackson, R. B. (2007). Toward an ecological classification of soil bacteria. Ecology, 88(6), 1354–1364. https://doi.org/10.1890/05-1839
- Gallardo-Cerda, J., Levihuan, J., Lavín, P., Oses, R., Atala, C., Torres-Díaz, C., Cuba-Díaz, M., Barrera, A., & Molina-Montenegro, M. A. (2018). Antarctic rhizobacteria improve salt tolerance and physiological performance of the Antarctic vascular plants. Polar Biology, 41, 1973–1982. https://doi.org/10.1007/s00300-018-2336-z
- Glick, B. R. (2005). Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiology Letters, 251(1), 1–7. https://doi.org/10.1016/j.femsle.2005.07.030
- Haichar, F. Z., Marol, C., Berge, O., Rangel-Castro, J. I., Prosser, J. I., Balesdent, J., Heulin, T., & Achouak, W. (2008). Plant host habitat and root exudates shape soil bacterial community structure. The ISME Journal, 2(12), 1221–1230. https://doi.org/10.1038/ismej.2008.80
- Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttilä, A. M., Compant, S., Campisano, A., Döring, M., & Sessitsch, A. (2015). The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews: MMBR, 79(3), 293–320. https://doi.org/10.1128/MMBR.00050-14
- Harris, J. M., & Tibbles, B. J. (1997). Factors affecting bacterial productivity in soils on isolated inland nunataks in continental Antarctica. Microbial Ecology, 33(2), 106–123. https://doi.org/10.1007/s002489900013
- Hereme, R., Morales-Navarro, S., Ballesteros, G., Barrera, A., Ramos, P., Gundel, P. E., & Molina-Montenegro, M. A. (2020). Fungal endophytes exert positive effects on Colobanthus quitensis under water stress but neutral under a projected climate change scenario in Antarctica. Frontiers in Microbiology, 11, 264. https://doi.org/10.3389/fmicb.2020.00264
- Komárková, V., Poncet, S., & Poncet, J. (1990). Additional and revisited localities of vascular plants Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl. in the Antarctic Peninsula area. Arctic and Alpine Research, 22(1), 108–113. https://doi.org/10.2307/1551725
- Lally, R. D., Galbally, P., Moreira, A. S., Spink, J., Ryan, D., Germaine, K. J., & Dowling, D. N. (2017). Application of endophytic Pseudomonas fluorescens and a bacterial consortium to Brassica napus can increase plant height and biomass under greenhouse and field conditions. Frontiers in Plant Science, 8, 2193. https://doi.org/10.3389/fpls.2017.02193
- Li, J., Wang, C., Liang, W., & Liu, S. (2021). Rhizosphere microbiome: the emerging barrier in plant-pathogen interactions. Frontiers in Microbiology, 12, 772420. https://doi.org/10.3389/fmicb.2021.772420
- Minamisawa, K., Nishioka, K., Miyaki, T., Ye, B., Miyamoto, T., You, M., Saito, A., Saito, M., Barraquio, W. L., Teaumroong, N., Sein, T., & Sato, T. (2004). Anaerobic nitrogen-fixing consortia consisting of clostridia isolated from gramineous plants. Applied and Environmental Microbiology, 70(5), 3096–3102. https://doi.org/10.1128/AEM.70.5.3096-3102.2004
- Miyamoto, T., Kawahara, M., & Minamisawa, K. (2004). Novel endophytic nitrogen-fixing clostridia from the grass Miscanthus sinensis as revealed by terminal restriction fragment length polymorphism analysis. Applied and Environmental Microbiology, 70(11), 6580–6586. https://doi.org/10.1128/AEM.70.11.6580-6586.2004
- Molina-Montenegro, M. A., Ballesteros, G. I., Castro-Nallar, E., Meneses, C., Gallardo-Cerda, J., & Torres-Díaz, C. (2019). A first insight into the structure and function of rhizosphere microbiota in Antarctic plants using shotgun metagenomic. Polar Biology, 42, 1825–1835. https://doi.org/10.1007/s00300-019-02556-7
- Naylor, D., DeGraaf, S., Purdom, E., & Coleman-Derr, D. (2017). Drought and host selection influence bacterial community dynamics in the grass root microbiome. The ISME Journal, 11(12), 2691–2704. https://doi.org/10.1038/ismej.2017.118
- Neu, A. T., Allen, E. E., & Roy, K. (2021). Defining and quantifying the core microbiome: Challenges and prospects. PNAS, 118(51), e2104429118. https://doi.org/10.1073/pnas.2104429118
- Peixoto, R. J. M., Miranda, K. R., Lobo, L. A., Granato, A., de Carvalho Maalouf, P., de Jesus, H. E., Rachid, C. T. C. C., Moraes, S. R., dos Santos, H. F., Peixoto, R. S., Rosado, A. S., & Domingues, R. M. C. P. (2016). Antarctic strict anaerobic microbiota from Deschampsia antarctica vascular plants rhizosphere reveals high ecology and biotechnology relevance. Extremophiles, 20, 875–884.https://doi.org/10.1007/s00792-016-0878-y
- Podolich, O., Prekrasna, I., Parnikoza, I., Voznyuk, T., Zubova, G., Zaets, I., Miryuta, N., Myryuta, G., Poronnik, O., Kozeretska, I., Kunakh, V., Pirttila, A. M., Dykyi, E., & Kozyrovska, N. (2021). First record of the endophytic bacteria of Deschampsia antarctica Ė. Desv. from two distant localities of the maritime Antarctic. Czech Polar Reports,11(1), 134–153. https://doi.org/10.5817/CPR2021-1-10
- Prekrasna, Ie., Dzhulai, A., & Parnikoza, I. (2021). Preliminary estimates of the number and diversity of the culturable endophytic bacteria from Deschampsia antarctica and Colobanthus quitensis. Bulletin of the Ukrainian Society of Geneticists and Breeders, 19(1–2), 21–30. https://doi.org/10.7124/visnyk.utgis.19.1-2.1437
- Prekrasna, I., Pavlovska, M., Miryuta, N., Dzhulai, A., Dykyi, E., Convey, P., Kozeretska, I., Bedernichek, T., & Parnikoza, I. (2022). Antarctic hairgrass rhizosphere microbiomes: microscale effects shape diversity, structure, and function. Microbes and Environment, 37(2), ME21069. https://doi.org/10.1264/jsme2.ME21069
- Ramos, P., Rivas, N., Pollmann, S., Casati, P., & Molina-Montenegro, M. A. (2018). Hormonal and physiological changes driven by fungal endophytes increase Antarctic plant performance under UV-B radiation. Fungal Ecology, 34, 76–82. https://doi.org/10.1016/j.funeco.2018.05.006
- Romera, F. J., García, M. J., Lucena, C., Martínez-Medina, A., Aparicio, M. A, Ramos, J., Alcántara, E., Angulo, M., & Pérez-Vicente, R. (2019). Induced Systemic Resistance (ISR) and Fe Deficiency Responses in Dicot Plants. Frontiers in Plant Science,10, 287. https://doi.org/10.3389/fpls.2019.00287
- Saito, A., Kawahara, M., Ikeda, S., Ishimine, M., Akao, S., & Minamisawa, K. (2008). Broad distribution and phylogeny of anaerobic endophytes of cluster XIVa clostridia in plant species including crops. Microbes and Environments, 23(1), 73–80. https://doi.org/10.1264/jsme2.23.73
- Santoyo, G., Moreno-Hagelsieb, G., Orozco-Mosqueda, M. C., & Glick, B. R. (2016). Plant growth-promoting bacterial endophytes. Microbiological Research,183, 92–99. https://doi.org/10.1016/j.micres.2015.11.008
- Sarria-Guzmán, Y., Chávez-Romero, Y., Gómez-Acata, S., Montes-Molina, J. A., Morales-Salazar, E., Dendooven, L., & Navarro-Noya, Y. E. (2016). Bacterial communities associated with different Anthurium andraeanum L. plant Tissues. Microbes and Environments, 31(3), 321–328. https://doi.org/10.1264/jsme2.ME16099
- Shi, Y., Yang, H., Chu, M., Niu, X., Wang, N., Lin, Q., Lou, K., Zuo, C., Wang, J., Zou, Q., & Zhang, Y. (2021). Differentiation and variability in the rhizosphere and endosphere microbiomes of healthy and diseased cotton (Gossypium sp.). Frontiers in Microbiology, 12, 765269. https://doi.org/10.3389/fmicb.2021.765269
- Singh, R. P., & Jha, P. N. (2017). The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in wheat plants. Frontiers in Microbiology, 8, 1945. https://doi.org/10.3389/fmicb.2017.01945
- Staebe, K., Meiklejohn, K. I., Singh, S. M., & Matcher, G. F. (2019). Biogeography of soil bacterial populations in the Jutulsessen and Ahlmannryggen of Western Dronning Maud Land, Antarctica. Polar Biology, 42, 1445–1458. https://doi.org/10.1007/s00300-019-02532-1
- Taketani, R. G., Lançoni, M. D., Kavamura, V. N., Durrer, A., Andreote, F. D., & Melo, I. S. (2017). Dry season constrains bacterial phylogenetic diversity in a semi-arid rhizosphere system. Microbial Ecology, 73, 153–161. https://doi.org/10.1007/s00248-016-0835-4
- Tamošiūnė, I., Stanienė, G., Haimi, P., Stanys, V., Rugienius, R., & Baniulis, D. (2018). Endophytic Bacillus and Pseudomonas spp. modulate apple shoot growth, cellular redox balance, and protein expression under in vitro conditions. Frontiers in Plant Science, 9, 889. https://doi.org/10.3389/fpls.2018.00889
- Tarquinio, F., Attlan, O., Vanderklift, M. A., Berry, O., & Bissett, A. (2021). Distinct endophytic bacterial communities inhabiting seagrass seeds. Frontiers in Microbiology, 12, 703014. https://doi.org/10.3389/fmicb.2021.703014
- Teixeira, L. C. R. S., Peixoto, R. S., Cury, J. C., Sul, W. J., Pellizari, V. H., Tiedje, J., & Rosado, A. S. (2010). Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. The ISME Journal, 4(8), 989–1001. https://doi.org/10.1038/ismej.2010.35
- Walters, W., Hyde, E. R., Berg-Lyons, D., Ackermann, G., Humphrey, G., Parada, A., Gilbert, J. A., Jansson, J. K., Capo Caporaso, J. G., Fuhrman, J. A., Apprill, A., & Knight, R. (2016). Improved bacterial 16S rRNA Gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems, 1(1), e00009-15. https://doi.org/10.1128/mSystems.00009-15
- Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261–5267. https://doi.org/10.1128/AEM.00062-07
- Williams, A., & de Vries, F. T. (2020). Plant root exudation under drought: implications for ecosystem functioning. New Phytologist, 225(5), 1899–1905. https://doi.org/10.1111/nph.16223
- Yergeau, E., Newsham, K. K., Pearce, D. A., & Kowalchuk, G. A. (2007). Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environmental Microbiology, 9(11), 2670–2682. https://doi.org/10.1111/j.1462-2920.2007.01379.x
- Yergeau, E., Bokhorst, S., Kang, S., Zhou, J., Greer, C. W., Aerts, R., & Kowalchuk, G. A. (2012). Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. The ISME Journal, 6(3), 692–702. https://doi.org/10.1038/ismej.2011.124
- Yue, H., Zhao, L., Yang, D., Zhang, M., Wu, J., Zhao, Z., Xing, X., Zhang, L., Qin, Y., Guo, F., Yang, J., & Aili, T. (2022). Comparative analysis of the endophytic bacterial diversity of Populus euphratica Oliv. in environments of different salinity intensities. Microbiology Spectrum, 10(3), e0050022. https://doi.org/10.1128/spectrum.00500-22
- Zhang, Q., Acuña, J. J., Inostroza, N. G., Mora, M. L., Radic, S., Sadowsky, M. J., & Jorquera, M. A. (2019). Endophytic bacterial communities associated with roots and leaves of plants growing in Chilean extreme environments. Scientific Reports, 9(1), 4950. https://doi.org/10.1038/s41598-019-41160-x
- Zhang, Q., Acuña, J. J., Inostroza, N. G., Duran, P., Mora, M. L., Sadowsky, M. J., & Jorquera, M. A. (2020). Niche differentiation in the composition, predicted function, and cooccurrence networks in bacterial communities associated with antarctic vascular plants. Frontiers in Microbiology, 11, 1036. https://doi.org/10.3389/fmicb.2020.01036
- Znój, A., Gawor, J., Gromadka, R., Chwedorzewska, K. J., & Grzesiak, J. (2022). Root-associated bacteria community characteristics of Antarctic plants: Deschampsia antarctica and Colobanthus quitensis – a Comparison. Microbial Ecology, 84(3), 808–820. https://doi.org/10.1007/s00248-021-01891-9
- Zuo, Y. W., Zhang, J. H., Ning, D. H., Zeng, Y. L., Li, W. Q., Xia, C. Y., Zhang, H., & Deng, H. P. (2022). Comparative analyses of rhizosphere bacteria along an elevational gradient of Thuja sutchuenensis. Frontiers in Microbiology, 13, 881921. https://doi.org/10.3389/fmicb.2022.881921