Soil microbiome after nine years of fly ash dump spontaneous revegetation
Natalia Naumova
A C , Ivan Belanov A , Tatiana Alikina B and Marsel Kabilov B
+ Author Affiliations
- Author Affiliations
A Institute of Soil Science and Agrochemistry, Siberian Branch of the Russian Academy of Sciences, Lavrentieva 8/2, Novosibirsk 620090, Russia.
B Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of Sciences, Lavrentieva 8, Novosibirsk 630090, Russia.
C Corresponding author. Email: naumova@issa-siberia.ru
Soil Research 59(7) 673-683 https://doi.org/10.1071/SR20304
Submitted: 2 November 2020 Accepted: 12 March 2021 Published: 18 June 2021
Abstract
Fly ash dumps of thermal power stations have been increasing in area worldwide due to the growing demand for power. One of the cost-effective approaches for restoring such sites is spontaneous revegetation in those areas where adjacent indigenous ecosystems can supply seeds and living organisms. We assessed microbiome taxonomic diversity in a Technosol developed during nine years of spontaneous revegetation of the terminated fly ash pond of a thermal power station in Novosibirsk, Russia, in comparison with microbiome diversity in undisturbed Phaeozem under adjacent birch forest by using 16S (V3–V4) and ITS2 (ITS3–ITS4) amplicon sequencing with Illumina MiSeq. We identified 577 fungal and 5542 bacterial operational taxonomic units (OTUs); 95–99% of them were minor or rare species. The dominant OTUs were completely different in the studied soils. At the phylum level, the ultimate dominants were Ascomycota (84%) in the Technosol and Basidiomycota (89%) in the Phaeozem. Three phyla (Proteobacteria, Acidobacteria and Actinobacteria), together comprising more than a half of the bacteriobiome, prevailed in both soils; however, at the OTU level, soil-related differences were found for 31% of the OTUs. The Technosol bacteriobiome was less structured and more diverse compared to the mycobiome, displaying the same phylum-level structure and OTU-based α-biodiversity as in the adjacent mature soil. Our finding that few fungal and bacterial OTUs dominated in the soil microbiome, the majority being minor or rare members, implies that key ecosystem processes performed by soil microorganisms rely on a very limited taxonomic diversity, both in young and mature soils.
Keywords: ITS DNA diversity, 16S rRNA gene diversity, Technosol, thermoelectric power station.
References
Abarenkov K, Zirk A, Piirmann T, Pöhönen R, Ivanov F, Nilsson RH, Kõljalg U (2020) UNITE USEARCH/UTAX release for Fungi Version 04.02.2020. [Dataset/DNA sequence] UNITE Community.Baldrian P, Větrovský T, Cajthaml T, Dobiášová P, Petránková M, Šnajdr J, et al (2013) Estimation of fungal biomass in forest litter and soil. Fungal Ecology 6, 1–11.
| Estimation of fungal biomass in forest litter and soil.Crossref | GoogleScholarGoogle Scholar |
Bayer-Santos E, Ceseti LdM, Farah CS, Alvarez-Martinez CE (2019) Distribution, Function and Regulation of Type 6 Secretion Systems of Xanthomonadales. Frontiers in Microbiology 10, 1635
| Distribution, Function and Regulation of Type 6 Secretion Systems of Xanthomonadales.Crossref | GoogleScholarGoogle Scholar | 31379785PubMed |
Cai Y, Zhang P, Liang J, Wang Q, Ding Y (2020) Power production waste. Water Environment Research 92, 1711–1716.
| Power production waste.Crossref | GoogleScholarGoogle Scholar | 32762097PubMed |
Calduch M, Gené J, Stchigel AM, Cano JF, Guarro J (2004) Ramophialophora, a new anamorphic genus of Sordariales. Studies in Mycology 50, 83–88.
Carter MR, Gregorich EG (2008) ‘Soil sampling and methods of analysis.’ (CRC Press: Boca Raton)
Castro-Silva C, Ruíz-Valdiviezo VM, Valenzuela-Encinas C (2013) The bacterial community structure in an alkaline saline soil spiked with anthracene. Electronic Journal of Biotechnology 16, 5
| The bacterial community structure in an alkaline saline soil spiked with anthracene.Crossref | GoogleScholarGoogle Scholar |
Challacombe JF, Hesse CN, Bramer LM, McCue LA, Lipton M, Purvine S, et al (2019) Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis. BMC Genomics 20, 976
| Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis.Crossref | GoogleScholarGoogle Scholar | 31830917PubMed |
Chen XW, Wong JT, Leung AO, Ng CW, Wong MH (2017) Comparison of plant and bacterial communities between a subtropical landfill topsoil 15 years after restoration and a natural area. Waste Management 63, 49–57.
| Comparison of plant and bacterial communities between a subtropical landfill topsoil 15 years after restoration and a natural area.Crossref | GoogleScholarGoogle Scholar | 27561244PubMed |
Daims H, Lücker S, Wagner M (2016) A New Perspective on Microbes Formerly Known as Nitrite-Oxidizing Bacteria. Trends in Microbiology 24, 699–712.
| A New Perspective on Microbes Formerly Known as Nitrite-Oxidizing Bacteria.Crossref | GoogleScholarGoogle Scholar | 27283264PubMed |
Das M, Agarwal P, Singh R, Adholeya A (2013) A study of abandoned ash ponds reclaimed through green cover development. International Journal of Phytoremediation 15, 320–329.
| A study of abandoned ash ponds reclaimed through green cover development.Crossref | GoogleScholarGoogle Scholar | 23487998PubMed |
Deshpande V, Wang Q, Greenfield P, Charleston M, Porras-Alfaro A, Kuske CR, et al (2016) Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia 108, 1–5.
| Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences.Crossref | GoogleScholarGoogle Scholar | 26553774PubMed |
Du C, Geng Z, Wang Q, Zhang T, He W, Hou L, et al (2017) Variations in bacterial and fungal communities through soil depth profiles in a Betula albosinensis forest. Journal of Microbiology (Seoul, Korea) 55, 684–693.
| Variations in bacterial and fungal communities through soil depth profiles in a Betula albosinensis forest.Crossref | GoogleScholarGoogle Scholar |
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads Nature Methods 10, 996–998.
| UPARSE: highly accurate OTU sequences from microbial amplicon readsCrossref | GoogleScholarGoogle Scholar | 23955772PubMed |
Edgar RC (2016 )
Egidi E, Delgado-Baquerizo M, Plett JM, Wang J, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK (2019) A few Ascomycota taxa dominate soil fungal communities worldwide. Nature Communications 10, 2369
| A few Ascomycota taxa dominate soil fungal communities worldwide.Crossref | GoogleScholarGoogle Scholar | 31147554PubMed |
Eichorst SA, Kuske CR (2012) Identification of Cellulose-Responsive Bacterial and Fungal Communities in Geographically and Edaphically Different Soils by Using Stable Isotope Probing. Applied and Environmental Microbiology 78, 2316–2327.
| Identification of Cellulose-Responsive Bacterial and Fungal Communities in Geographically and Edaphically Different Soils by Using Stable Isotope Probing.Crossref | GoogleScholarGoogle Scholar | 22287013PubMed |
Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, et al (2014) An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6
| An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform.Crossref | GoogleScholarGoogle Scholar | 24558975PubMed |
Fuentes A, Herrera H, Charles TC, Arriagada C (2020) Fungal and Bacterial Microbiome Associated With the Rhizosphere of Native Plants From the Atacama Desert. Microorganisms 8, 209
| Fungal and Bacterial Microbiome Associated With the Rhizosphere of Native Plants From the Atacama Desert.Crossref | GoogleScholarGoogle Scholar |
Garrido-Oter R, Nakano RT, Dombrowski N, Ma KW, The AgBiome Team McHardy AC, et al (2018) Modular Traits of the Rhizobiales Root Microbiota and Their Evolutionary Relationship with Symbiotic Rhizobia. Cell Host & Microbe 24, 155–167.e5.
| Modular Traits of the Rhizobiales Root Microbiota and Their Evolutionary Relationship with Symbiotic Rhizobia.Crossref | GoogleScholarGoogle Scholar |
Gleason FH, Letcher PM, McGee PA (2004) Some Chytridiomycota in soil recover from drying and high temperatures. Mycological Research 108, 583–589.
| Some Chytridiomycota in soil recover from drying and high temperatures.Crossref | GoogleScholarGoogle Scholar | 15230008PubMed |
Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4, 9
Haynes RJ (2009) Reclamation and revegetation of fly ash disposal sites - Challenges and research needs. Journal of Environmental Management 2009, 43–53.
| Reclamation and revegetation of fly ash disposal sites - Challenges and research needs.Crossref | GoogleScholarGoogle Scholar |
Hughes JB, Hellmann JJ (2005) The Application of Rarefaction Techniques to Molecular Inventories of Microbial Diversity. Methods in Enzymology 397, 292–308.
| The Application of Rarefaction Techniques to Molecular Inventories of Microbial Diversity.Crossref | GoogleScholarGoogle Scholar | 16260298PubMed |
Igolkina AA, Grekhov GA, Pershina EV, Samosorova GG, Leunova VM, Semenova AN, et al (2018) Identifying components of mixed and contaminated soil samples by detecting specific signatures of control 16S rRNA libraries. Ecological Indicators 94, 446–453.
| Identifying components of mixed and contaminated soil samples by detecting specific signatures of control 16S rRNA libraries.Crossref | GoogleScholarGoogle Scholar |
IUSS Working Group (2015) ‘WRB, World Reference Base for Soil Resources 2014, update 2015: International soil classification system for naming soils and creating legends for soil maps.’ (FAO: Rome)
Jambhulkar HP, Shaikh SMS, Kumar MS (2018) Fly ash toxicity, emerging issues and possible implications for its exploitation in agriculture; Indian scenario: A review. Chemosphere 213, 333–344.
| Fly ash toxicity, emerging issues and possible implications for its exploitation in agriculture; Indian scenario: A review.Crossref | GoogleScholarGoogle Scholar | 30241077PubMed |
Jomura M, Kuwayama T, Soma Y, Yamaguchi M, Komatsu M, Maruyama Y (2020) Mycelial biomass estimation and metabolic quotient of Lentinula edodes using species-specific qPCR. PLoS One 15, e0232049
| Mycelial biomass estimation and metabolic quotient of Lentinula edodes using species-specific qPCR.Crossref | GoogleScholarGoogle Scholar | 32421692PubMed |
Kim SJ, Ahn JH, Lee TH, Weon HY, Hong SB, Seok SJ, et al. (2013) Reyranella soli sp. nov., isolated from forest soil, and emended description of the genus Reyranella Pagnier et al. 2011. International Journal of Systematic and Evolutionary Microbiology 63, 3164–3167.
| Reyranella soli sp. nov., isolated from forest soil, and emended description of the genus Reyranella Pagnier et al. 2011.Crossref | GoogleScholarGoogle Scholar | 23435248PubMed |
Kim B-R, Shin J, Guevarra RB, Lee JH, Kim DW, Seol K-H, Lee J-H, Kim HB, Isaacson RE (2017) Deciphering Diversity Indices for a Better Understanding of Microbial Communities. Journal of Microbiology and Biotechnology 27, 2089–2093.
| Deciphering Diversity Indices for a Better Understanding of Microbial Communities.Crossref | GoogleScholarGoogle Scholar | 29032640PubMed |
Koizumi T, Nara K (2017) Communities of Putative Ericoid Mycorrhizal Fungi Isolated from Alpine Dwarf Shrubs in Japan: Effects of Host Identity and Microhabitat. Microbes and Environments 32, 147–153.
| Communities of Putative Ericoid Mycorrhizal Fungi Isolated from Alpine Dwarf Shrubs in Japan: Effects of Host Identity and Microhabitat.Crossref | GoogleScholarGoogle Scholar | 28529264PubMed |
Lovley DR, Walker DJF (2019) Geobacter Protein Nanowires. Frontiers in Microbiology 10, 2078
| Geobacter Protein Nanowires.Crossref | GoogleScholarGoogle Scholar | 31608018PubMed |
Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, et al (2011) Geobacter: the microbe electric’s physiology, ecology, and practical applications. Advances in Microbial Physiology 59, 1–100.
| Geobacter: the microbe electric’s physiology, ecology, and practical applications.Crossref | GoogleScholarGoogle Scholar | 22114840PubMed |
Maiti D, Prasad B (2016) revegetation of fly ash – a review with emphasis on grass-legume plantation and bioaccumulation of metals. Applied Ecology and Environmental Research 14, 185–212.
| revegetation of fly ash – a review with emphasis on grass-legume plantation and bioaccumulation of metals.Crossref | GoogleScholarGoogle Scholar |
Marchesi JR, Ravel J (2015) The vocabulary of microbiome research: a proposal. Microbiome 3, 31
| The vocabulary of microbiome research: a proposal.Crossref | GoogleScholarGoogle Scholar | 26229597PubMed |
Matić S, Gilardi G, Gullino ML, Garibaldi A (2019) Emergence of leaf spot disease on leafy vegetable and ornamental crops caused by Paramyrothecium and Albifimbria species. Phytopathology 109, 1053–1061.
| Emergence of leaf spot disease on leafy vegetable and ornamental crops caused by Paramyrothecium and Albifimbria species.Crossref | GoogleScholarGoogle Scholar | 30667339PubMed |
Midgley DJ, Letcher PM, McGee PA (2006) Access to organic and insoluble sources of phosphorus varies among soil Chytridiomycota. Archives of Microbiology 186, 211–217.
| Access to organic and insoluble sources of phosphorus varies among soil Chytridiomycota.Crossref | GoogleScholarGoogle Scholar | 16868741PubMed |
Moubasher AH, Ismail MA, Al-Bedak OA, Mohamed RA (2019) Ramophialophora chlamydospora, a new species from an alkaline lake of Wadi-El-Natron, Egypt. Asian Journal of Mycology 2, 110–117.
| Ramophialophora chlamydospora, a new species from an alkaline lake of Wadi-El-Natron, Egypt.Crossref | GoogleScholarGoogle Scholar |
Murgia M, Fiamma M, Barac A, Deligios M, Mazzarello V, Paglietti B, et al (2019) Biodiversity of fungi in hot desert sands. MicrobiologyOpen 8, e00595
| Biodiversity of fungi in hot desert sands.Crossref | GoogleScholarGoogle Scholar | 29504263PubMed |
Palomo ADechesne ASmets BF (2019 )
Ram LC, Masto RE (2010) An appraisal of the potential use of fly ash for reclaiming coal mine spoil. Journal of Environmental Management 91, 603–617.
| An appraisal of the potential use of fly ash for reclaiming coal mine spoil.Crossref | GoogleScholarGoogle Scholar | 19914766PubMed |
Shaheen SM, Hooda PS, Tsadilas CD (2014) Opportunities and challenges in the use of coal fly ash for soil improvements - a review. Journal of Environmental Management 145, 249–267.
| Opportunities and challenges in the use of coal fly ash for soil improvements - a review.Crossref | GoogleScholarGoogle Scholar | 25079682PubMed |
Sheremet NVBelanov IPDoronkin VLamanova TNaumova NB (2018 )
Shishov LL, Tonkonogov VD, Lebedeva II, Gerasimova MI (2004) ‘Classification and diagnostics of soils in Russia.’ (Oykumena Publishers: Moscow) [in Russian]
Smith ML, Bruhn JN, Anderson JB (1992) The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356, 428–431.
| The fungus Armillaria bulbosa is among the largest and oldest living organisms.Crossref | GoogleScholarGoogle Scholar |
Song Z, Vail A, Sadowsky MJ, Schilling JS (2014) Quantitative PCR for measuring biomass of decomposer fungi in planta. Fungal Ecology 7, 39–46.
| Quantitative PCR for measuring biomass of decomposer fungi in planta.Crossref | GoogleScholarGoogle Scholar |
Strom N, Hu W, Haarith D, Chen S, Bushley K (2020) Interactions between soil properties, fungal communities, the soybean cyst nematode, and crop yield under continuous corn and soybean monoculture. Applied Soil Ecology 147, 103388
| Interactions between soil properties, fungal communities, the soybean cyst nematode, and crop yield under continuous corn and soybean monoculture.Crossref | GoogleScholarGoogle Scholar |
Usmani Z, Kumar V, Pratishtha Gupta P, Gupta G, Rani R, Chandra A (2019) Enhanced soil fertility, plant growth promotion and microbial enzymatic activities of vermicomposted fly ash. Scientific Reports 9, 10455
| Enhanced soil fertility, plant growth promotion and microbial enzymatic activities of vermicomposted fly ash.Crossref | GoogleScholarGoogle Scholar | 31320739PubMed |
VanInsberghe D, Maas KR, Cardenas E, Strachan CR, Hallam SJ, Mohn WW (2015) Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils. The ISME Journal 9, 2435–2441.
| Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils.Crossref | GoogleScholarGoogle Scholar | 25909973PubMed |
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy. Applied and Environmental Microbiology 73, 5261–5267.
| Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy.Crossref | GoogleScholarGoogle Scholar | 17586664PubMed |
Wu S, You F, Wu Z, Bond P, Hall M, Huang L (2020) Molecular diversity of arbuscular mycorrhizal fungal communities across the gradient of alkaline Fe ore tailings, revegetated waste rock to natural soil sites. Environmental Science and Pollution Research International 27, 11968–11979.
| Molecular diversity of arbuscular mycorrhizal fungal communities across the gradient of alkaline Fe ore tailings, revegetated waste rock to natural soil sites.Crossref | GoogleScholarGoogle Scholar | 31983001PubMed |
Zhang ZF, Liu F, Zho X, Liu XZ, Liu SJ, Cai L (2017) Culturable mycobiota from Karst caves in China, with descriptions of 20 new species. Persoonia 39, 1–31.
| Culturable mycobiota from Karst caves in China, with descriptions of 20 new species.Crossref | GoogleScholarGoogle Scholar | 29503468PubMed |
