Abstract
The permafrost in the polar regions is vital for maintaining the status quo of the earth’s climate by limiting greenhouse gas emissions. The present study aims to investigate the seasonal variations and the influence of physicochemical parameters on the bacterial diversity and community structure of active layer permafrost (AL) around Ny-Ålesund, Svalbard. The AL soil samples were collected from four different geographical locations around Ny-Ålesund during the winter and summer seasons. The 16S rDNA amplicon sequencing was carried out to investigate the diversity and distribution profiles of bacterial communities among the collected AL samples. Physico-chemical parameters including soil pH, moisture content, total carbon (TC), total nitrogen (TN), and trace metals concentrations were measured. Bacterial phyla, Proteobacteria (15.4%–26%) and Chloroflexi (9.6%–22.5%) were predominantly distributed across both seasons. In the winter samples, Verrucomicrobiota (14.12%–23.39%) phylum, consisting of genera Chthoniobacter and Opitutus were highly abundant (Lefse, p < 0.05), whereas in summer bacterial genera belonging to Gemmatimonadota (3.3%–13.74%) and Acidobacteriota (18.02%–28.52%) phyla were highly abundant. The bacterial richness and diversity index were not significantly different between the winter and summer seasons. Principal coordinate analysis (PCoA) has revealed a distinct grouping between two seasons (PERMANOVA, p < 0.05). Bacterial community structure was significantly varied between winter and summer seasons, whereas the physico-chemical variable, TN, influenced the community structure. About 37.8% of the total operational taxonomic units (OTUs) were shared between seasons, whereas 25.4% and 36.8% of OTUs were unique to the summer and winter seasons. The present study revealed that the conditions prevailing during winter and summer has shaped bacterial community structure in AL samples albeit the stable diversity and most of the variation was explained by TN, indicating its critical role in oligotrophic permafrost.
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Data availability
Generated sequence data submitted to NCBI-Sequence Read Archive (SRA) with the Accession Number: PRJNA719032.
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References
Antonelli F, Esposito A, Calvo L et al (2020) Characterization of black patina from the tiber river embankments using next-generation sequencing. PLoS One 15:e0227639. https://doi.org/10.1371/journal.pone.0227639
Beckers B, De Beeck MO, Weyens N et al (2017) Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees. Microbiome 5(1):1–17
Beermann F, Langer M, Wetterich S et al (2017) Permafrost thaw and liberation of inorganic nitrogen in Eastern Siberia. Permafr Periglac Process 28:605–618. https://doi.org/10.1002/ppp.1958
Brewer TE, Handley KM, Carini P et al (2017) Genome reduction in an abundant and ubiquitous soil bacterium “Candidatus Udaeobacter copiosus”. Nat Microbiol 2:16198. https://doi.org/10.1038/nmicrobiol.2016.198
Buckeridge KM, Banerjee S, Siciliano SD, Grogan P (2013) The seasonal pattern of soil microbial community structure in mesic low arctic tundra. Soil Biol Biochem 65:338–347. https://doi.org/10.1016/j.soilbio.2013.06.012
Chin KJ, Liesack W, Janssen PH (2001) Opitutus terrae gen. nov., sp. nov., to accommodate novel strains of the division “Verrucomicrobia” isolated from rice paddy soil. Int J Syst Evol Microbiol 51:1965–1968. https://doi.org/10.1099/00207713-51-6-1965
Chu H, Fierer N, Lauber CL et al (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12:2998–3006. https://doi.org/10.1111/j.1462-2920.2010.02277.x
Colatriano D, Tran PQ, Guéguen C et al (2018) Genomic evidence for the degradation of terrestrial organic matter by pelagic Arctic Ocean chloroflexi bacteria. Commun Biol 1:90. https://doi.org/10.1038/s42003-018-0086-7
Coyotzi S, Doxey AC, Clark ID et al (2017) Agricultural soil denitrifiers possess extensive nitrite reductase gene diversity. Environ Microbiol 19:1189–1208. https://doi.org/10.1111/1462-2920.13643
Crevecoeur S, Vincent WF, Lovejoy C (2016) Environmental selection of planktonic methanogens in permafrost thaw ponds. Sci Rep 6:31312. https://doi.org/10.1038/srep31312
Dedysh SN, Kulichevskaya IS, Huber KJ, Overmann J (2017) Defining the taxonomic status of described subdivision 3 Acidobacteria: proposal of Bryobacteraceae fam. nov. Int J Syst Evol Microbiol 67:498–501. https://doi.org/10.1099/ijsem.0.001687
Eckerstorfer M, Christiansen HH (2011) The “high Arctic maritime snow climate” in central Svalbard. Arctic, Antarct Alp Res 43:11–21. https://doi.org/10.1657/1938-4246-43.1.11
Feng J, Wang C, Lei J et al (2020) Warming-induced permafrost thaw exacerbates tundra soil carbon decomposition mediated by microbial community. Microbiome 8:3. https://doi.org/10.1186/s40168-019-0778-3
Frank-Fahle BA, Yergeau É, Greer CW et al (2014) Microbial functional potential and community composition in permafrost-affected soils of the NW Canadian Arctic. PLoS One 9:e84761. https://doi.org/10.1371/journal.pone.0084761
Gentsch N, Wild B, Mikutta R et al (2018) Temperature response of permafrost soil carbon is attenuated by mineral protection. Glob Chang Biol 24:3401–3415. https://doi.org/10.1111/gcb.14316
Górniak D, Marszałek H, Kwaśniak-Kominek M et al (2017) Soil formation and initial microbiological activity on a foreland of an Arctic glacier (SW Svalbard). Appl Soil Ecol 114:34–44. https://doi.org/10.1016/j.apsoil.2017.02.017
Gruber S (2012) Derivation and analysis of a high-resolution estimate of global permafrost zonation. Cryosph 6:221–233. https://doi.org/10.5194/tc-6-221-2012
Hanssen-Bauer I, Førland EJ, Hisdal H et al (2019) Climate in Svalbard 2100.
Hayes DJ, Kicklighter DW, McGuire AD et al (2014) The impacts of recent permafrost thaw on land–atmosphere greenhouse gas exchange. Environ Res Lett 9:045005. https://doi.org/10.1088/1748-9326/9/4/045005
Hugelius G, Strauss J, Zubrzycki S et al (2014) Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11:6573–6593. https://doi.org/10.5194/bg-11-6573-2014
Humlum O, Instanes A, Sollid JL (2003) Permafrost in Svalbard: a review of research history, climatic background and engineering challenges. Polar Res 22:191–215. https://doi.org/10.1111/j.1751-8369.2003.tb00107.x
Ivanova AA, Zhelezova AD, Chernov TI, Dedysh SN (2020) Linking ecology and systematics of acidobacteria: Distinct habitat preferences of the Acidobacteriia and Blastocatellia in tundra soils. PLoS ONE 15:e0230157. https://doi.org/10.1371/journal.pone.0230157
Jiang S, Liu X, Sun J et al (2011) A multi-proxy sediment record of late holocene and recent climate change from a lake near Ny-Ålesund, Svalbard. Boreas 40:468–480. https://doi.org/10.1111/j.1502-3885.2010.00198.x
Kant R, van Passel MWJ, Palva A et al (2011) Genome sequence of Chthoniobacter flavus Ellin428, an aerobic heterotrophic soil bacterium. J Bacteriol 193:2902–2903. https://doi.org/10.1128/JB.00295-11
Kielak AM, Barreto CC, Kowalchuk GA et al (2016) The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 7:1–16. https://doi.org/10.3389/fmicb.2016.00744
Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13
Lapébie P, Lombard V, Drula E et al (2019) Bacteroidetes use thousands of enzyme combinations to break down glycans. Nat Commun 10:2043. https://doi.org/10.1038/s41467-019-10068-5
Lindström ES, Kamst-Van Agterveld MP, Zwart G (2005) Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol 71:8201–8206. https://doi.org/10.1128/AEM.71.12.8201-8206.2005
Lipson DA, Monson RK (1998) Plant-microbe competition for soil amino acids in the alpine tundra: effects of freeze-thaw and dry-rewet events. Oecologia 113:406–414. https://doi.org/10.1007/s004420050393
Mackelprang R, Saleska SR, Jacobsen CS et al (2016) Permafrost meta-omics and climate change. Annu Rev Earth Planet Sci 44:439–462. https://doi.org/10.1146/annurev-earth-060614-105126
McMahon SK, Wallenstein MD, Schimel JP (2011) A cross-seasonal comparison of active and total bacterial community composition in Arctic tundra soil using bromodeoxyuridine labeling. Soil Biol Biochem 43:287–295. https://doi.org/10.1016/j.soilbio.2010.10.013
McMurdie PJ, Holmes S (2013) phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217
Navarrete AA, Kuramae EE, de Hollander M et al (2013) Acidobacterial community responses to agricultural management of soybean in Amazon forest soils. FEMS Microbiol Ecol 83:607–621. https://doi.org/10.1111/1574-6941.12018
Neina D (2019) The role of soil pH in plant nutrition and soil remediation. Appl Environ Soil Sci 2019:1–9. https://doi.org/10.1155/2019/5794869
Park D, Kim H, Yoon S (2017) Nitrous oxide reduction by an obligate aerobic bacterium, Gemmatimonas aurantiaca Strain T-27. Appl Environ Microbiol 83:e00502-e517. https://doi.org/10.1128/AEM.00502-17
Quast C, Pruesse E, Yilmaz P et al (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
Sarneel JM, Sundqvist MK, Molau U et al (2020) Decomposition rate and stabilization across six tundra vegetation types exposed to >20 years of warming. Sci Total Environ 724:138304. https://doi.org/10.1016/j.scitotenv.2020.138304
Schimel JP, Clein JS (1996) Microbial response to freeze-thaw cycles in tundra and taiga soils. Soil Biol Biochem 28:1061–1066. https://doi.org/10.1016/0038-0717(96)00083-1
Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Schostag M, Stibal M, Jacobsen CS et al (2015) Distinct summer and winter bacterial communities in the active layer of Svalbard permafrost revealed by DNA- and RNA-based analyses. Front Microbiol 6:399. https://doi.org/10.3389/fmicb.2015.00399
Shi Y, Xiang X, Shen C et al (2015) Vegetation-associated impacts on arctic tundra bacterial and microeukaryotic communities. Appl Environ Microbiol 81:492–501. https://doi.org/10.1128/AEM.03229-14
Strand SM, Christiansen HH, Johansson M et al (2021) Active layer thickening and controls on interannual variability in the Nordic Arctic compared to the circum-Arctic. Permafr Periglac Process 32:47–58. https://doi.org/10.1002/ppp.2088
Szekeres S, Kiss I, Kalman M, Soares MIM (2002) Microbial population in a hydrogen-dependent denitrification reactor. Water Res 36:4088–4094. https://doi.org/10.1016/S0043-1354(02)00130-6
Szymański W, Drewnik M, Stolarczyk M et al (2022) Occurrence and stability of organic intercalation in clay minerals from permafrost-affected soils in the High Arctic – A case study from Spitsbergen (Svalbard). Geoderma 408:115591. https://doi.org/10.1016/j.geoderma.2021.115591
Takahashi S, Tomita J, Nishioka K et al (2014) Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS ONE 9:e105592. https://doi.org/10.1371/journal.pone.0105592
Thomas FA, Sinha RK, Krishnan KP (2020) Bacterial community structure of a glacio-marine system in the Arctic (Ny-Ålesund, Svalbard). Sci Total Environ 718:135264. https://doi.org/10.1016/j.scitotenv.2019.135264
Tveit A, Schwacke R, Svenning MM, Urich T (2013) Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. ISME J 7:299–311. https://doi.org/10.1038/ismej.2012.99
Venkatachalam S, Kannan VM, Saritha VN et al (2021) Bacterial diversity and community structure along the glacier foreland of Midtre Lovénbreen, Svalbard. Arctic Ecol Indic 126:107704. https://doi.org/10.1016/j.ecolind.2021.107704
Wallenstein MD, McMahon S, Schimel J (2007) Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiol Ecol 59:428–435. https://doi.org/10.1111/j.1574-6941.2006.00260.x
Willms IM, Rudolph AY, Göschel I et al (2020) Globally Abundant “Candidatus Udaeobacter” benefits from release of antibiotics in soil and potentially performs trace gas scavenging. mSphere 5:e00186. https://doi.org/10.1128/mSphere.00186-20
Wu M, Huang H, Li G et al (2017) The evolutionary life cycle of the polysaccharide biosynthetic gene cluster based on the Sphingomonadaceae. Sci Rep 7:46484. https://doi.org/10.1038/srep46484
Zeng Y, Koblížek M (2017) Phototrophic Gemmatimonadetes: A new “purple” branch on the bacterial tree of life. modern topics in the phototrophic prokaryotes. Springer International Publishing, Cham, pp 163–192
Zhou L, Zhou Y, Yao X et al (2020a) Decreasing diversity of rare bacterial subcommunities relates to dissolved organic matter along permafrost thawing gradients. Environ Int 134:105330. https://doi.org/10.1016/j.envint.2019.105330
Zhou Z, Yu M, Ding G et al (2020b) Diversity and structural differences of bacterial microbial communities in rhizocompartments of desert leguminous plants. PloS One 15(12):e0241057
Acknowledgements
The authors wish to express their gratitude to Director, NCPOR for his support and encouragement. This work was carried out as a part of the Indian scientific expedition to the Arctic-2019. We also thank Dr. N.S. Magesh, NCPOR, for his assistance in the map generation and Dr. P. Ashok, IIT Hyderabad for CHN analysis. This is NCPOR contribution number J-66/2021-22.
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National Centre for Polar and Ocean Research, Ministry of Earth Sciences (Govt. of India).
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DSL: Conceptualization; Sample collection; Data curation; Formal analysis; Investigation; Methodology; Writing—original draft, SV: Formal analysis; Writing—review & editing, TJ: Sample collection; Formal analysis, PV: Sample collection; Formal analysis and KPK: Supervision; Funding acquisition; Writing—review & editing. All authors read and approved the manuscript.
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Loganathachetti, D.S., Venkatachalam, S., Jabir, T. et al. Total nitrogen influence bacterial community structure of active layer permafrost across summer and winter seasons in Ny-Ålesund, Svalbard. World J Microbiol Biotechnol 38, 28 (2022). https://doi.org/10.1007/s11274-021-03210-3
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DOI: https://doi.org/10.1007/s11274-021-03210-3