Humic substance turnover by bacterial decomposers in the maritime Antarctic soil
Dockyu Kim
A B * , Mincheol Kim A B , Sungho Woo A , Eungbin Kim C and Hyoungseok Lee A B
A
B
C
Abstract
Soil fungi and bacteria play a crucial role in decomposing soil organic matter (SOM) and providing nutrients to terrestrial ecosystems. However, in polar environments, their relative contributions to decomposition remain unclear.
This study aimed to determine whether fungi or bacteria contributes more to humic substances (HS) decomposition (the largest constituent of SOM) in maritime Antarctic soils under controlled laboratory conditions with elevated temperature and moisture levels.
Soil culturing method was used to select for soil microbes that efficiently degrade HS. During culturing at 18°C for 30 days, Antarctic soils were treated with selective antimicrobials to manipulate microbial communities. After culturing, HS degradation and bacterial communities were analysed. The effects of soil culturing on plant growth were also evaluated using Arabidopsis thaliana as a surrogate for Antarctic plants.
HS decomposition and solubilisation were more pronounced in antifungal-treated soils compared to antibacterial-treated soils. Antifungal treatment reduced bacterial alpha diversity, altered bacterial composition, and increased the abundance of rhizosphere-associated Saccharibacteria. Bacterial growth resumed quickly after antibacterial treatment indicating resilience to antimicrobials. Soil culturing resulted in a higher water-soluble HS fraction, which significantly enhanced the fresh and dry weights of A. thaliana.
Antarctic bacteria exhibit higher degradative activity and resilience to antimicrobials compared to fungi, promoting HS decomposition and solubilisation. This indicates that bacteria have a greater impact on Antarctic soil functioning than fungi.
These findings highlight the critical role of bacteria in nutrient cycling and plant growth in polar ecosystems.
Keywords: Antarctic tundra, bacterial decomposers, dissolved organic matter, fungal decomposers, global warming, humic substances, plant growth promotion, solubilisation.
References
Abakumov E, Alekseev I (2018) Stability of soil organic matter in Cryosols of the maritime Antarctic: insights from 13C NMR and electron spin resonance spectroscopy. Solid Earth 9(6), 1329-1339.
| Crossref | Google Scholar |
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26(1), 32-46.
| Crossref | Google Scholar |
Aqeel M, Ran J, Hu W, Irshad MK, Dong L, Akram MA, Eldesoky GE, Aljuwayid AM, Chuah LF, Deng J (2023) Plant-soil-microbe interactions in maintaining ecosystem stability and coordinated turnover under changing environmental conditions. Chemosphere 318, 137924.
| Crossref | Google Scholar | PubMed |
Bölter M (2011) Soil development and soil biology on King George Island, maritime Antarctic. Polish Polar Research 32(2), 105-116.
| Crossref | Google Scholar |
Boyle SA, Yarwood RR, Bottomley PJ, Myrold DD (2008) Bacterial and fungal contributions to soil nitrogen cycling under Douglas fir and red alder at two sites in Oregon. Soil Biology and Biochemistry 40(2), 443-451.
| Crossref | Google Scholar |
Bromwich DH, Nicolas JP, Monaghan AJ, Lazzara MA, Keller LM, Weidner GA, Wilson AB (2014) Corrigendum: Central West Antarctica among the most rapidly warming regions on Earth. Nature Geoscience 7(1), 76.
| Crossref | Google Scholar |
Byun MY, Kim D, Youn UJ, Lee S, Lee H (2021) Improvement of moss photosynthesis by humic acids from Antarctic tundra soil. Plant Physiology and Biochemistry 159, 37-42.
| Crossref | Google Scholar | PubMed |
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods 13(7), 581-583.
| Crossref | Google Scholar | PubMed |
Deflandre B, Gagné J-P (2001) Estimation of dissolved organic carbon (DOC) concentrations in nanoliter samples using UV spectroscopy. Water Research 35(13), 3057-3062.
| Crossref | Google Scholar | PubMed |
Frey B, Rime T, Phillips M, Stierli B, Hajdas I, Widmer F, Hartmann M (2016) Microbial diversity in European alpine permafrost and active layers. FEMS Microbiology Ecology 92(3), fiw018.
| Crossref | Google Scholar |
Husain H, Keitel C, Dijkstra FA (2024) Fungi are more important than bacteria for soil carbon loss through priming effects and carbon protection through aggregation. Applied Soil Ecology 195, 105245.
| Crossref | Google Scholar |
Johnston ER, Hatt JK, He Z, Wu L, Guo X, Luo Y, Schuur EAG, Tiedje JM, Zhou J, Konstantinidis KT (2019) Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths. Proceedings of the National Academy of Sciences 116(30), 15096-15105.
| Crossref | Google Scholar |
Kim D, Lee H (2019) Draft genome sequence of humic substance-degrading Pseudomonas sp. PAMC 29040 from Antarctic tundra soil. Korean Journal of Microbiology 49(1), 83-85.
| Crossref | Google Scholar |
Kim D, Park HJ, Kim JH, Youn UJ, Yang YH, Casanova-Katny A, Vargas CM, Venegas EZ, Park H, Hong SG (2018) Passive warming effect on soil microbial community and humic substance degradation in maritime Antarctic region. Journal of Basic Microbiology 58(6), 513-522.
| Crossref | Google Scholar | PubMed |
Kim M, Lim H-S, Hyun C-U, Cho A, Noh H-J, Hong SG, Kim O-S (2019) Local-scale variation of soil bacterial communities in ice-free regions of maritime Antarctica. Soil Biology and Biochemistry 133, 165-173.
| Crossref | Google Scholar |
Kim D, Park HJ, Kim M, Lee S, Hong SG, Kim E, Lee H (2022a) Temperature sensitivity of Antarctic soil-humic substance degradation by cold-adapted bacteria. Environmental Microbiology 24(1), 265-275.
| Crossref | Google Scholar |
Kim D, Chae N, Kim M, Nam S, Kim TK, Park K-T, Lee BY, Kim E, Lee H (2022b) Microbial metabolic responses and CO2 emissions differentiated by soil water content variation in subarctic tundra soils. Journal of Microbiology 60(12), 1130-1138.
| Crossref | Google Scholar |
Kulikova NA, Perminova IV (2021) Interactions between humic substances and microorganisms and their implications for nature-like bioremediation technologies. Molecules 26(9), 2706.
| Crossref | Google Scholar |
Leenheer JA, Croue J-P (2003) Characterizing aquatic dissolved organic matter. Environmental Science & Technology 37(1), 18A-26A.
| Crossref | Google Scholar | PubMed |
Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528(7580), 60-68.
| Crossref | Google Scholar | PubMed |
Lipczynska-Kochany E (2018) Humic substances, their microbial interactions and effects on biological transformations of organic pollutants in water and soil: a review. Chemosphere 202, 420-437.
| Crossref | Google Scholar | PubMed |
Luo L, Meng H, Gu J-D (2017) Microbial extracellular enzymes in biogeochemical cycling of ecosystems. Journal of Environmental Management 197, 539-549.
| Crossref | Google Scholar | PubMed |
Lupatini M, Suleiman AKA, Jacques RJS, Lemos LN, Pylro VS, Van Veen JA, Kuramae EE, Roesch LFW (2019) Moisture is more important than temperature for assembly of both potentially active and whole prokaryotic communities in subtropical grassland. Microbial Ecology 77(2), 460-470.
| Crossref | Google Scholar | PubMed |
Ma S, Zhu W, Wang W, Li X, Sheng Z (2023) Microbial assemblies with distinct trophic strategies drive changes in soil microbial carbon use efficiency along vegetation primary succession in a glacier retreat area of the southeastern Tibetan Plateau. Science of the Total Environment 867, 161587.
| Crossref | Google Scholar | PubMed |
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal 17(1), 10-12.
| Crossref | Google Scholar |
Matus F, Mendoza D, Nájera F, Merino C, Kuzyakov Y, Wilhelm K, Boy J, Aburto F, Jofré I, Dippold MA (2023) Freezing–thawing cycles affect organic matter decomposition in periglacial maritime Antarctic soils. Biogeochemistry 163(3), 311-325.
| Crossref | Google Scholar |
Nardi S, Muscolo A, Vaccaro S, Baiano S, Spaccini R, Piccolo A (2007) Relationship between molecular characteristics of soil humic fractions and glycolytic pathway and krebs cycle in maize seedlings. Soil Biology and Biochemistry 39(12), 3138-3146.
| Crossref | Google Scholar |
Park HJ, Kim D (2015) Isolation and characterization of humic substances-degrading bacteria from the subarctic Alaska grasslands. Journal of Basic Microbiology 55(1), 54-61.
| Crossref | Google Scholar | PubMed |
Park HJ, Chae N, Sul WJ, Lee BY, Lee YK, Kim D (2015) Temporal changes in soil bacterial diversity and humic substances degradation in subarctic tundra soil. Microbial Ecology 69(3), 668-675.
| Crossref | Google Scholar | PubMed |
Pizzeghello D, Schiavon M, Francioso O, Dalla Vecchia F, Ertani A, Nardi S (2020) Bioactivity of size-fractionated and unfractionated humic substances from two forest soils and comparative effects on N and S metabolism, nutrition, and root anatomy of Allium sativum L. Frontiers in Plant Science 11, 1203.
| Crossref | Google Scholar | PubMed |
Pradel P, Bravo LA, Merino C, Trefault N, Rodríguez R, Knicker H, Jara C, Larama G, Matus F (2023) Microbial response to warming and cellulose addition in a maritime Antarctic soil. Permafrost and Periglacial Processes 2023, 1-14.
| Crossref | Google Scholar |
Rousk J, Demoling LA, Bååth E (2009) Contrasting short-term antibiotic effects on respiration and bacterial growth compromises the validity of the selective respiratory inhibition technique to distinguish fungi and bacteria. Microbial Ecology 58(1), 75-85.
| Crossref | Google Scholar | PubMed |
Rüthi J, Bölsterli D, Pardi-Comensoli L, Brunner I, Frey B (2020) The “plastisphere” of biodegradable plastics is characterized by specific microbial taxa of alpine and arctic soils. Frontiers in Environmental Science 8, 562263.
| Crossref | Google Scholar |
Semedo M, Song B, Sparrer T, Phillips RL (2018) Antibiotic effects on microbial communities responsible for denitrification and N2O production in grassland soils. Frontiers in Microbiology 9, 2121.
| Crossref | Google Scholar | PubMed |
Soares M, Rousk J (2019) Microbial growth and carbon use efficiency in soil: links to fungal-bacterial dominance, SOC-quality and stoichiometry. Soil Biology and Biochemistry 131, 195-205.
| Crossref | Google Scholar |
Spaccini R, Piccolo A, Conte P, Haberhauer G, Gerzabek MH (2002) Increased soil organic carbon sequestration through hydrophobic protection by humic substances. Soil Biology and Biochemistry 34(12), 1839-1851.
| Crossref | Google Scholar |
Starr EP, Shi SJ, Blazewicz SJ, Probst AJ, Herman DJ, Firestone MK, Banfield JF (2018) Stable isotope informed genome-resolved metagenomics reveals that Saccharibacteria utilize microbially-processed plant-derived carbon. Microbiome 6(1), 122.
| Crossref | Google Scholar |
Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils – methods, controls, and ecosystem implications. Soil Biology and Biochemistry 42(9), 1385-1395.
| Crossref | Google Scholar |
Swallow MJB, Quideau SA (2020) Evidence of rapid non-targeted effects of cycloheximide on soil bacteria using 13C-PLFA analysis. Canadian Journal of Soil Science 100(4), 356-362.
| Crossref | Google Scholar |
Trevisan S, Francioso O, Quaggiotti S, Nardi S (2010) Humic substances biological activity at the plant-soil interface: from environmental aspects to molecular factors. Plant Signaling & Behavior 5(6), 635-643.
| Crossref | Google Scholar | PubMed |
Tripathi BM, Kim M, Kim Y, Byun E, Yang J-W, Ahn J, Lee YK (2018) Variations in bacterial and archaeal communities along depth profiles of Alaskan soil cores. Scientific Reports 8(1), 504.
| Crossref | Google Scholar | PubMed |
Ueno A, Shimizu S, Tamamura S, Okuyama H, Naganuma T, Kaneko K (2016) Anaerobic decomposition of humic substances by Clostridium from the deep subsurface. Scientific Reports 6, 18990.
| Crossref | Google Scholar | PubMed |
Ushio M, Miki T, Balser TC (2013) A coexisting fungal-bacterial community stabilizes soil decomposition activity in a microcosm experiment. PLoS ONE 8(11), e80320.
| Crossref | Google Scholar | PubMed |
Wicaksono JA, Purwadaria T, Yulandi A, Tan WA (2022) Bacterial dynamics during the burial of starch-based bioplastic and oxo-low-density-polyethylene in compost soil. BMC Microbiology 22(1), 309.
| Crossref | Google Scholar | PubMed |
Yergeau E, Bokhorst S, Huiskes AHL, Boschker HTS, Aerts R, Kowalchuk GA (2007) Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbiology Ecology 59(2), 436-451.
| Crossref | Google Scholar | PubMed |
Yergeau E, Bokhorst S, Kang S, Zhou J, Greer CW, Aerts R, Kowalchuk GA (2012) Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. The ISME Journal 6(3), 692-702.
| Crossref | Google Scholar | PubMed |
Zanin L, Tomasi N, Cesco S, Varanini Z, Pinton R (2019) Humic substances contribute to plant iron nutrition acting as chelators and biostimulants. Frontiers in Plant Science 10, 675.
| Crossref | Google Scholar | PubMed |
