Abstract
There is considerable interest in understanding the processes of microbial development in volcanic ash. We tested the predictions that there would be (1) a distinctive bacterial community associated with soil development on volcanic ash, including groups previously implicated in weathering studies; (2) a slower increase in bacterial abundance and soil C and N accumulation in cooler climates; and (3) a distinct communities developing on the same substrate in different climates. We set up an experiment, taking freshly fallen, sterilized volcanic ash from Sakurajima volcano, Japan. Pots of ash were positioned in multiple locations, with mean annual temperature (MAT) ranging from 18.6 to −3 °C. Within 12 months, bacteria were detectable by qPCR in all pots. By 24 months, bacterial copy numbers had increased by 10–100 times relative to a year before. C and N content approximately doubled between 12 and 24 months. HiSeq and MiSeq sequencing of the 16S rRNA gene revealed a distinctive bacterial community, different from developed vegetated soils in the same areas, for example in containing an abundance of unclassified bacterial groups. Community composition also differed between the ash pots at different sites, while showing no pattern in relation to MAT. Contrary to our predictions, the bacterial abundance did not show any relation to MAT. It also did not correlate to pH or N, and only C was statistically significant. It appears that bacterial community development on volcanic ash can be a rapid process not closely sensitive to temperature, involving distinct communities from developed soils.
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References
Leamy M, Smith G, Colmet-Daage F, Otowa M (1984) The morphological characteristics of Andisols 34–51
Shoji S, Nanzyo M, Dahlgren R (1994) Volcanic ash soils: genesis, properties and utilization. Elsevier
Ugolini FC, Dahlgren RA (2002) Soil development in volcanic ash. Global Environ Res English Edition 6:69–82
Tsai C, Chen Z, Kao C, Ottner F, Kao S, Zehetner F (2010) Pedogenic development of volcanic ash soils along a climosequence in northern Taiwan. Geoderma 156:48–59
Duchauffour P (1977) Pédogénèse et classification. Masson, Paris
Berner RA (1991) A model for atmospheric CO sub 2 over phanerozoic time. Am J Sci (US) 291
Dessert C, Dupré B, Gaillardet J, François LM, Allegre CJ (2003) Basalt weathering laws and the impact of basalt weathering on the global carbon cycle. Chem Geol 202:257–273
White AF, Blum AE, Bullen TD, Vivit DV, Schulz M, Fitzpatrick J (1999) The effect of temperature on experimental and natural chemical weathering rates of granitoid rocks. Geochim Cosmochim Acta 63:3277–3291. doi:10.1016/S0016-7037(99)00250-1
Gislason SR, Oelkers EH, Eiriksdottir ES, Kardjilov MI, Gisladottir G, Sigfusson B, Snorrason A, Elefsen S, Hardardottir J, Torssander P (2009) Direct evidence of the feedback between climate and weathering. Earth Planet Sci Lett 277:213–222
Huh Y (2003) Chemical weathering and climate—a global experiment: a review. Geosci J 7:277–288
Aomine S, Wada K (1962) Differential weathering of volcanic ash and pumice, resulting in formation of hydrated halloysite. Am Mineral 47:1024–1048
Zambell C, Adams J, Gorring M, Schwartzman D (2012) Effect of lichen colonization on chemical weathering of hornblende granite as estimated by aqueous elemental flux. Chem Geol 291:166–174
Gleeson DB, Kennedy NM, Clipson N, Melville K, Gadd GM, McDermott FP (2006) Characterization of bacterial community structure on a weathered pegmatitic granite. Microb Ecol 51:526–534
Lu H, Sato Y, Fujimura R, Nishizawa T, Kamijo T, Ohta H (2011) Limnobacter litoralis sp. nov., a thiosulfate-oxidizing, heterotrophic bacterium isolated from a volcanic deposit, and emended description of the genus Limnobacter. Int J Syst Evol Microbiol 61: 404–407
Sato Y, Hosokawa K, Fujimura R, Nishizawa T, Kamijo T, Ohta H (2009) Nitrogenase activity (acetylene reduction) of an iron-oxidizing Leptospirillum strain cultured as a pioneer microbe from a recent volcanic deposit on Miyake-jima, Japan. Microbes Environ 24:291–296
Fujimura R, Sato Y, Nishizawa T, Nanba K, Oshima K, Hattori M, Kamijo T, Ohta H (2012) Analysis of early bacterial communities on volcanic deposits on the island of Miyake (Miyake-jima), Japan: a 6-year study at a fixed site. Microbes Environ 27:19–29
Cockell CS, Kelly L, Summers S (2011) Microbiology of volcanic environments. Extremophiles handbook. Springer, pp. 917–933
Gomez-Alvarez V, King GM, Nüsslein K (2007) Comparative bacterial diversity in recent Hawaiian volcanic deposits of different ages. FEMS Microbiol Ecol 60:60–73
Hernández M, Dumont MG, Calabi M, Basualto D, Conrad R (2014) Ammonia oxidizers are pioneer microorganisms in the colonization of new acidic volcanic soils from South of Chile. Environ Microbiol Rep 6:70–79
King GM (2003) Contributions of atmospheric CO and hydrogen uptake to microbial dynamics on recent Hawaiian volcanic deposits. Appl Environ Microbiol 69:4067–4075
Wall DH, Virginia RA (1999) Controls on soil biodiversity: insights from extreme environments. Appl Soil Ecol 13:137–150
Dunfield KE, King GM (2004) Molecular analysis of carbon monoxide-oxidizing bacteria associated with recent Hawaiian volcanic deposits. Appl Environ Microbiol 70:4242–4248
Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24:133–141
Uroz S, Calvaruso C, Turpault M-P, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387
Kawano M, Tomita K (2001) Microbial biomineralization in weathered volcanic ash deposit and formation of biogenic minerals by experimental incubation. Am Mineral 86:400–410
Urakawa R, Shibata H, Kuroiwa M, Inagaki Y, Tateno R, Hishi T, Fukuzawa K, Hirai K, Toda H, Oyanagi N (2014) Effects of freeze–thaw cycles resulting from winter climate change on soil nitrogen cycling in ten temperate forest ecosystems throughout the Japanese archipelago. Soil Biol Biochem 74:82–94
Bonan G (2015) Ecological climatology: concepts and applications. Cambridge University Press
Iwatsuki Z, Mizutani M (1972) Coloured illustrations of bryophytes of Japan. Hoikusha, Osaka
Asahina Y (1956) Lichens of Japan: Nihon No Chii. Research Institute for Natural Resources
Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4, e1000255
Zhou HW, Li DF, Tam NF, Jiang XT, Zhang H, Sheng HF, Qin J, Liu X, Zou F (2011) BIPES, a cost-effective high-throughput method for assessing microbial diversity. ISME J 5:741–749. doi:10.1038/ismej.2010.160
Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09
Chun J, Lee J-H, Jung Y, Kim M, Kim S, Kim BK, Lim Y-W (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261
Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898. doi:10.1111/j.1462-2920.2010.02193.x
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Felsenstein J (1985) Confidence limits on phylogenies with a molecular clock. Syst Biol 34:152–161
Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinf 9:386
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens M, Oksanen M, Suggests M (2007) The vegan package. Community ecology package
Cossins A (2012) Temperature biology of animals. Springer Science & Business Media
Zuo W, Moses ME, West GB, Hou C, Brown JH (2012) A general model for effects of temperature on ectotherm ontogenetic growth and development. Proc R Soc Lond B Biol Sci 279:1840–1846
Brady PV, Carroll SA (1994) Direct effects of CO 2 and temperature on silicate weathering: possible implications for climate control. Geochim Cosmochim Acta 58:1853–1856
Hartmann J, Moosdorf N, Lauerwald R, Hinderer M, West AJ (2014) Global chemical weathering and associated P-release—the role of lithology, temperature and soil properties. Chem Geol 363:145–163
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems; with 47 tables. Springer Science & Business Media
Stretch R, Viles H (2002) The nature and rate of weathering by lichens on lava flows on Lanzarote. Geomorphology 47:87–94
Singh D, Lee-Cruz L, Kim W-S, Kerfahi D, Chun J-H, Adams JM (2014) Strong elevational trends in soil bacterial community composition on Mt. Halla, South Korea. Soil Biol Biochem 68:140–149
Singh D, Takahashi K, Kim M, Chun J, Adams JM (2012) A hump-backed trend in bacterial diversity with elevation on Mount Fuji, Japan. Microb Ecol 63:429–437
Singh D, Takahashi K, Adams JM (2012) Elevational patterns in archaeal diversity on Mt Fuji. PLoS One 7(9), e44494
Chen M-M, Zhu Y-G, Su Y-H, Chen B-D, Fu B-J, Marschner P (2007) Effects of soil moisture and plant interactions on the soil microbial community structure. Eur J Soil Biol 43:31–38
Zogg GP, Zak DR, Ringelberg DB, White DC, MacDonald NW, Pregitzer KS (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J61:475–481
Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007
Lipson D, Schadt C, Schmidt S (2002) Changes in soil microbial community structure and function in an alpine dry meadow following spring snow melt. Microb Ecol 43:307–314
Zhang B, Liang C, He H, Zhang X (2013) Variations in soil microbial communities and residues along an altitude gradient on the northern slope of Changbai Mountain, China. PLoS One 8(6), e66184
Zeglin L, Rainey F, Wang B, Waythomas C, Talbot S (2013) Soil microbial structure and function post-volcanic eruption on Kasatochi Island and regional controls on microbial heterogeneity. AGU Fall Meet Abstr 1:0322
Liu L, Gundersen P, Zhang T, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38
Tripathi BM, Kim M, Lai-Hoe A, Shukor NA, Rahim RA, Go R, Adams JM (2013) pH dominates variation in tropical soil archaeal diversity and community structure. FEMS Microbiol Ecol 86:303–311
Preem J-K, Truu J, Truu M, Mander Ü, Oopkaup K, Lõhmus K, Helmisaari H-S, Uri V, Zobel M (2012) Bacterial community structure and its relationship to soil physico-chemical characteristics in alder stands with different management histories. Ecol Eng 49:10–17
Cai W-J, Guo X, Chen C-TA, Dai M, Zhang L, Zhai W, Lohrenz SE, Yin K, Harrison PJ, Wang Y (2008) A comparative overview of weathering intensity and HCO 3− flux in the world’s major rivers with emphasis on the Changjiang, Huanghe, Zhujiang (Pearl) and Mississippi Rivers. Cont Shelf Res 28:1538–1549
Acknowledgments
This work was supported by a grant from the National Research Foundation (NRF) funded by the Korean government, Ministry of Education, Science and Technology (MEST) (NRF-0409-20150076).
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Kerfahi, D., Tateno, R., Takahashi, K. et al. Development of Soil Bacterial Communities in Volcanic Ash Microcosms in a Range of Climates. Microb Ecol 73, 775–790 (2017). https://doi.org/10.1007/s00248-016-0873-y
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DOI: https://doi.org/10.1007/s00248-016-0873-y