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Metagenome Across a Geochemical Gradient of Indian Stone Ruins Found at Historic Sites in Tamil Nadu, India

  • Environmental Microbiology
  • Published:
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Abstract

Although stone surfaces seem unlikely to be habitable, they support microbial life. Life on these surfaces are subjected to many varying harsh conditions and require the inhabitants to exhibit resistance to environmental factors including UV irradiation, toxic metal exposure, and fluctuating temperatures and humidity. Here we report the effect of hosting stone geochemistry on the microbiome of stone ruins found in Tamil Nadu, India. The microbial communities found on the two lithologies, granite and granodiorite, hosted distinct populations of bacteria. Geochemical composition analysis of sampled stones revealed quartz mineral content as a major driver of microbial community structure, particularly promoting community richness and proportions of Cyanobacteria and Deinococcus-Thermus. Other geochemical parameters including ilmenite, albite, anorthite, and orthoclase components or elemental concentrations (Ti, Fe, Mn, Na, and K) also influenced community structure to a lesser degree than quartz. Core members of the stone microbiome community found on both lithologies were also identified and included Cyanobacteria (Chroococcidiopsaceae and Dapisostemonum CCIBt 3536), Rubrobacter, and Deinococcus. A cluster of taxa including Sphingomonas, Geodermatophilus, and Truepera were mostly found in the granodiorite samples. Community diversity correlated with quartz mineral content in these samples may indicate that the microbial communities that attach to quartz surfaces may be transient and regularly changing. This work has expanded our understanding of built-stone microbial community structure based on lithology and geochemistry.

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Data availability

All sequence data (16S rRNA gene datasets) presented in this article is available in the repository of NCBI under Bioproject number PRJNA545121.

References

  1. Warscheid T (1996) Impacts of microbial biofilms in the deterioration of inroganic building materials and their relevance for conservation practice. Internationale Zeitschrift fur Bauinstandsetzen 2:493–504

    Google Scholar 

  2. May E, Papida S, Abdulla H, Tayler S, Dewedar A (2000) Comparative studies of microbial communities on stone monuments in temperate and semi-arid climates. In: Ciferri O, Tiano P, Mastromei G (eds) Of microbes and art: the role of microbial communities in the degradation and protection of cultural heritage. Kluwer Academic Publishers, New York, pp 49–62

    Chapter  Google Scholar 

  3. Cockell CS, Rettberg P, Horneck G, Wynn-Williams DD, Scherer K, Gugg-Helminger A (2002) Influence of ice and snow covers on the UV exposure of terrestrial microbial communities: dosimetric studies. J Photochem Photobiol B 68:23–32. https://doi.org/10.1016/S1011-1344(02)00327-5

    Article  CAS  PubMed  Google Scholar 

  4. Gtari M, Essoussi I, Maaoui R, Sghaier H, Boujmil R, Gury J, Pujic P, Brusetti L, Chouaia B, Crotti E, Daffonchio D, Boudabous A, Normand P (2012) Contrasted resistance of stone-dwelling Geodermatophilaceae species to stresses known to give rise to reactive oxygen species. FEMS Microbiol Ecol 80:566–577. https://doi.org/10.1111/j.1574-6941.2012.01320.x

    Article  CAS  PubMed  Google Scholar 

  5. Gorbushina AA, Krumbein WE, Volkmann M (2002) Rock surfaces as life indicators: new ways to demonstrate life and traces of former life. Astrobiology 2:203–213. https://doi.org/10.1089/15311070260192273

    Article  CAS  PubMed  Google Scholar 

  6. Zanardini E, Andreoni V, Borin S, Cappitelli F, Daffonchio D, Talotta P, Sorlini C, Ranalli G, Bruni S, Cariati F (1997) Lead-resistant microorganisms from red stains of marble of the Certosa of Pavia, Italy and use of nucleic acid-based techniques for their detection. Int Biodeterior Biodegradation 40:171–182. https://doi.org/10.1016/S0964-8305(97)00057-7

    Article  CAS  Google Scholar 

  7. Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631. https://doi.org/10.1111/j.1462-2920.2007.01301.x

    Article  CAS  PubMed  Google Scholar 

  8. Louati M, Ennis NJ, Ghodhbane-Gtari F, Hezbri K, Sevigny JL, Fahnestock MF, Cherif-Silini H, Bryce JG, Tisa LS, Gtari M (2020) Elucidating the ecological networks in stone-dwelling microbiomes. Environ Microbiol 22:1467–1480. https://doi.org/10.1111/1462-2920.14700

    Article  CAS  PubMed  Google Scholar 

  9. Gaylarde C, Ogawa A, Beech I, Kowalski M, Baptista-Neto JA (2017) Analysis of of dark crusts on the church of Nossa Senhora do Carmo in Rio de Janeiro, Brazil, using chemical, microscope and metabarcoding microbial identification techniques. Int Biodeterior Biodegradation 117:60–67. https://doi.org/10.1016/j.ibiod.2016.11.028

    Article  CAS  Google Scholar 

  10. Gaylarde C, Baptista-Neto JA, Ogawa A, Kowalski M, Celikkol-Aydin S, Beech I (2017) Epilithic and endolithic microorganisms and deterioration on stone church facades subject to urban pollution in a sub-tropical climate. Biofouling 33:113–127. https://doi.org/10.1080/08927014.2016.1269893

    Article  PubMed  Google Scholar 

  11. Ortega-Morales BO, Gaylarde CC, Englert GE, Gaylarde PM (2005) Analysis of salt-containing biofilms on limestone buildings of the Mayan culture at Edzna, Mexico. Geomicrobiol J 22:261–268. https://doi.org/10.1080/01490450500182524

    Article  CAS  Google Scholar 

  12. Urzi C, Realini M (1998) Colour changes of Noto’s calcareous sandstone as related to its colonisation by microorganisms. Int Biodeterior Biodegradation 42:45–54. https://doi.org/10.1016/S0964-8305(98)00045-6

    Article  Google Scholar 

  13. Gadd GM (2017) Geomicrobiology of the built environment. Nat Microbiol 2:16275. https://doi.org/10.1038/nmicrobiol.2016.275

    Article  CAS  PubMed  Google Scholar 

  14. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108. https://doi.org/10.1038/nrmicro821

    Article  CAS  PubMed  Google Scholar 

  15. Kemmling A, Kamper M, Flies C, Schieweck O, Hoppert M (2004) Biofilms and extracellular matrices on geomaterials. Environ Geol 46:429–435. https://doi.org/10.1007/s00254-004-1044-x

    Article  CAS  Google Scholar 

  16. Sterflinger K, Krumbein WE (1995) Multiple stress factors affecting growth of rock-inhabiting black fungi. Bot Acta 108:490–496. https://doi.org/10.1111/j.1438-8677.1995.tb00526.x

    Article  Google Scholar 

  17. Abdulla H (2009) Bioweathering and biotransformation of granitic rock minerals by Actinomycetes. Microb Ecol 58:753–761. https://doi.org/10.1007/s00248-009-9549-1

    Article  CAS  PubMed  Google Scholar 

  18. Cockell CS, Kelly LC, Marteinsson V (2013) Actinobacteria—an ancient phylum active in volcanic rock weathering. Geomicrobiol J 30:706–720. https://doi.org/10.1080/01490451.2012.758196

    Article  CAS  Google Scholar 

  19. Kiel G, Gaylarde CC (2006) Bacterial diversity in biofilms on external surfaces of historic buildings in Porto Alegre. World J Microbiol Biotechnol 22:293–297. https://doi.org/10.1007/s11274-005-9035-y

    Article  Google Scholar 

  20. Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Petrol 51:475–478

    Google Scholar 

  21. Ortega-Morales O, Guezennec J, Hernandez-Duque G, Gaylarde CC, Gaylarde PM (2000) Phototrophic biofilms on ancient Mayan buildings in Yucatan, Mexico. Curr Microbiol 40:81–85. https://doi.org/10.1007/s002849910015

    Article  CAS  PubMed  Google Scholar 

  22. Saizjimenez C, Garciarowe J, Delcura MAG, Ortega-Calvo JJ, Roekens E, Vangrieken R (1990) Endolithic Cyanobacteria in Maastricht Limestone. Sci Total Environ 94:209–220. https://doi.org/10.1016/0048-9697(90)90171-P

    Article  CAS  Google Scholar 

  23. Urzi C, Brusetti L, Salamone P, Sorlini C, Stackebrandt E, Daffonchio D (2001) Biodiversity of Geodermatophilaceae isolated from altered stones and monuments in the Mediterranean basin. Environ Microbiol 3:471–479. https://doi.org/10.1046/j.1462-2920.2001.00217.x

    Article  CAS  PubMed  Google Scholar 

  24. Scheerer S, Ortega-Morales O, Gaylarde C (2009) Microbial deterioration of stone monuments—an updated overview. Adv Appl Microbiol 66:97–139. https://doi.org/10.1016/S0065-2164(08)00805-8

    Article  CAS  PubMed  Google Scholar 

  25. Meslier V, Casero MC, Dailey M, Wierzchos J, Ascaso C, Artieda O, McCullough PR, DiRuggiero J (2018) Fundamental drivers for endolithic microbial community assemblies in the hyperarid Atacama Desert. Environ Microbiol 20:1765–1781. https://doi.org/10.1111/1462-2920.14106

    Article  PubMed  Google Scholar 

  26. Borin S, Ventura S, Tambone F, Mapelli F, Schubotz F, Brusetti L, Scaglia B, D'Acqui LP, Solheim B, Turicchia S, Marasco R, Hinrichs KU, Baldi F, Adani F, Daffonchio D (2010) Rock weathering creates oases of life in a High Arctic desert. Environ Microbiol 12:293–303. https://doi.org/10.1111/j.1462-2920.2009.02059.x

    Article  CAS  PubMed  Google Scholar 

  27. Normand P, Daffonchio D, Gtari M (2014) The family Geodermatophilaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin, pp 361–379

    Google Scholar 

  28. Hezbri K, Ghodhbane-Gtari F, Montero-Calasanz MD, Nouioui I, Rohde M, Spoer C, Schumann P, Klenk HP, Gtari M (2016) Geodermatophilus pulveris sp nov., a gamma-radiation-resistant actinobacterium isolated from the Sahara desert. Int J Syst Evol Microbiol 66:3828–3834. https://doi.org/10.1099/ijsem.0.001272

    Article  CAS  PubMed  Google Scholar 

  29. Hezbri K, Ghodhbane-Gtari F, Montero-Calasanz MD, Sghaier H, Rohde M, Schumann P, Klenk HP, Gtari M (2015) Geodermatophilus sabuli sp nov., a gamma-radiation-resistant actinobacterium isolated from desert limestone. Int J Syst Evol Microbiol 65:3365–3372. https://doi.org/10.1099/ijsem.0.000422

    Article  CAS  PubMed  Google Scholar 

  30. Hezbri K, Ghodhbane-Gtari F, Montero-Calasanz MD, Sghaier H, Rohde M, Schumann P, Klenk HP, Gtari M (2015) Description of Geodermatophilus bullaregiensis sp nov. Anton Leeuw Int J G 108:415–425. https://doi.org/10.1007/s10482-015-0494-3

    Article  CAS  Google Scholar 

  31. Hezbri K, Ghodhbane-Gtari F, Montero-Calasanz MD, Sghaier H, Rohde M, Sproer C, Schumann P, Klenk HP, Gtari M (2015) Geodermatophilus aquaeductus sp nov., isolated from the ruins of Hadrian’s aqueduct. Anton Leeuw Int J G 108:41–50. https://doi.org/10.1007/s10482-015-0461-z

    Article  CAS  Google Scholar 

  32. Montero-Calasanz MD, Hofner B, Goker M, Rohde M, Sproer C, Hezbri K, Gtari M, Schumann P, Klenk HP (2014) Geodermatophilus poikilotrophi sp nov.: a multitolerant actinomycete isolated from dolomitic marble. Biomed Res Int: Artn 914767. https://doi.org/10.1155/2014/914767

  33. Montero-Calasanz MD, Hezbri K, Goker M, Sghaier H, Rohde M, Sproer C, Schumann P, Klenk HP (2015) Description of gamma radiation-resistant Geodermatophilus dictyosporus sp nov to accommodate the not validly named Geodermatophilus obscurus subsp dictyosporus (Luedemann, 1968). Extremophiles 19:77–85. https://doi.org/10.1007/s00792-014-0708-z

    Article  CAS  Google Scholar 

  34. Cockell CS, Olsson K, Knowles F, Kelly L, Herrera A, Thorsteinsson T, Marteinsson V (2009) Bacteria in weathered basaltic glass, Iceland. Geomicrobiol J 26:491–507. https://doi.org/10.1080/01490450903061101

    Article  CAS  Google Scholar 

  35. Gorbushina AA, Krumbein WE (2004) Role of organisms in wear down of rocks and minerals. In: Buscot F, Varma A (eds) Micro-organisms in soils:roles in genesis and function. Springer, Berlin

    Google Scholar 

  36. Bennett PC, Melcer ME, Siegel DI, Hassett JP (1988) The dissolution of quartz in dilute aqueous-solutions of organic-acids at 25-degrees-C. Geochim Cosmochim Acta 52:1521–1530. https://doi.org/10.1016/0016-7037(88)90222-0

    Article  CAS  Google Scholar 

  37. Young ME, Urquhart DCM (1998) Algal growth on building sandstones: effects of chemical stone cleaning methods. Q J Eng Geol Hydrogeol 31:315–324. https://doi.org/10.1144/Gsl.Qjeg.1998.031.P4.04

    Article  Google Scholar 

  38. Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Koppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. https://doi.org/10.5194/hess-11-1633-2007

    Article  Google Scholar 

  39. World weather online. 2018

  40. Frey FA, Rhodes JM, Cox KG, McKenzie DP, White RS (1993) Intershield geochemical differences among Hawaiian volcanoes: implications for source compositions, melting process and magma ascent paths. Philos Trans R Soc Lond Ser A Phys Eng Sci 342:121–136. https://doi.org/10.1098/rsta.1993.0009

    Article  CAS  Google Scholar 

  41. Kelsey CH (1965) Calculation of Cipw norm. Mineral Mag J Mineral Soc 34:276. https://doi.org/10.1180/minmag.1965.034.268.23

    Article  CAS  Google Scholar 

  42. Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, Prill RJ, Tripathi A, Gibbons SM, Ackermann G, Navas-Molina JA, Janssen S, Kopylova E, Vazquez-Baeza Y, Gonzalez A, Morton JT, Mirarab S, Xu ZZ, Jiang LJ, Haroon MF, Kanbar J, Zhu QJ, Song SJ, Kosciolek T, Bokulich NA, Lefler J, Brislawn CJ, Humphrey G, Owens SM, Hampton-Marcell J, Berg-Lyons D, McKenzie V, Fierer N, Fuhrman JA, Clauset A, Stevens RL, Shade A, Pollard KS, Goodwin KD, Jansson JK, Gilbert JA, Knight R, Rivera JLA, Al-Moosawi L, Alverdy J, Amato KR, Andras J, Angenent LT, Antonopoulos DA, Apprill A, Armitage D, Ballantine K, Barta J, Baum JK, Berry A, Bhatnagar A, Bhatnagar M, Biddle JF, Bittner L, Boldgiv B, Bottos E, Boyer DM, Braun J, Brazelton W, Brearley FQ, Campbell AH, Caporaso JG, Cardona C, Carroll J, Cary SC, Casper BB, Charles TC, Chu HY, Claar DC, Clark RG, Clayton JB, Clemente JC, Cochran A, Coleman ML, Collins G, Colwell RR, Contreras M, Crary BB, Creer S, Cristol DA, Crump BC, Cui DY, Daly SE, Davalos L, Dawson RD, Defazio J, Delsuc F, Dionisi HM, Dominguez-Bello MG, Dowell R, Dubinsky EA, Dunn PO, Ercolini D, Espinoza RE, Ezenwa V, Fenner N, Findlay HS, Fleming ID, Vincenzo F, Forsman A, Freeman C, Friedman ES, Galindo G, Garcia L, Garcia-Amado MA, Garshelis D, Gasser RB, Gerdts G, Gibson MK, Gifford I, Gill RT, Giray T, Gittel A, Golyshin P, Gong DL, Grossart HP, Guyton K, Haig SJ, Hale V, Hall RS, Hallam SJ, Handley KM, Hasan NA, Haydon SR, Hickman JE, Hidalgo G, Hofmockel KS, Hooker J, Hulth S, Hultman J, Hyde E, Ibanez-Alamo JD, Jastrow JD, Jex AR, Johnson LS, Johnston ER, Joseph S, Jurburg SD, Jurelevicius D, Karlsson A, Karlsson R, Kauppinen S, Kellogg CTE, Kennedy SJ, Kerkhof LJ, King GM, Kling GW, Koehler AV, Krezalek M, Kueneman J, Lamendella R, Landon EM, Lane-deGraaf K, LaRoche J, Larsen P, Laverock B, Lax S, Lentino M, Levin II, Liancourt P, Liang WJ, Linz AM, Lipson DA, Liu YQ, Lladser ME, Lozada M, Spirito CM, MacCormack WP, MacRae-Crerar A, Magris M, Martin-Platero AM, Martin-Vivaldi M, Martinez LM, Martinez-Bueno M, Marzinelli EM, Mason OU, Mayer GD, McDevitt-Irwin JM, McDonald JE, McGuire KL, McMahon KD, McMinds R, Medina M, Mendelson JR, Metcalf JL, Meyer F, Michelangeli F, Miller K, Mills DA, Minich J, Mocali S, Moitinho-Silva L, Moore A, Morgan-Kiss RM, Munroe P, Myrold D, Neufeld JD, Ni YY, Nicol GW, Nielsen S, Nissimov JI, Niu KF, Nolan MJ, Noyce K, O'Brien SL, Okamoto N, Orlando L, Castellano YO, Osuolale O, Oswald W, Parnell J, Peralta-Sanchez JM, Petraitis P, Pfister C, Pilon-Smits E, Piombino P, Pointing SB, Pollock FJ, Potter C, Prithiviraj B, Quince C, Rani A, Ranjan R, Rao S, Rees AP, Richardson M, Riebesell U, Robinson C, Rockne KJ, Rodriguezl SM, Rohwer F, Roundstone W, Safran RJ, Sangwan N, Sanz V, Schrenk M, Schrenzel MD, Scott NM, Seger RL, Seguin-Orlando A, Seldin L, Seyler LM, Shakhsheer B, Sheets GM, Shen CC, Shi Y, Shin HD, Shogan BD, Shutler D, Siegel J, Simmons S, Sjoling S, Smith DP, Soler JJ, Sperling M, Steinberg PD, Stephens B, Stevens MA, Taghavi S, Tai V, Tait K, Tan CL, Tas N, Taylor DL, Thomas T, Timling I, Turner BL, Urich T, Ursell LK, van der Lelie D, Van Treuren W, van Zwieten L, Vargas-Robles D, Thurber RV, Vitaglione P, Walker DA, Walters WA, Wang S, Wang T, Weaver T, Webster NS, Wehrle B, Weisenhorn P, Weiss S, Werner JJ, West K, Whitehead A, Whitehead SR, Whittingham LA, Willerslev E, Williams AE, Wood SA, Woodhams DC, Yang YQ, Zaneveld J, Zarraonaindia I, Zhang QK, Zhao HX, Consortiu EMP (2017) A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551:457. https://doi.org/10.1038/nature24621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581. https://doi.org/10.1038/Nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Nguyen NP, Warnow T, Pop M, White B (2016) A perspective on 16S rRNA operational taxonomic unit clustering using sequence similarity. Npj Biofilms Microbi 2: Unsp 16004. https://doi.org/10.1038/Npjbiofilms.2016.4

  46. Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2 ' s q2-feature-classifier plugin. Microbiome 6: ARTN 90. https://doi.org/10.1186/s40168-018-0470-z

  47. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) 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

    Article  CAS  PubMed  Google Scholar 

  48. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. Plos One 8:e61217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vazquez-Baeza Y, Birmingham A, Hyde ER, Knight R (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:ARTN 27

    Article  Google Scholar 

  50. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:623–656. https://doi.org/10.1002/j.1538-7305.1948.tb00917.x

    Article  Google Scholar 

  51. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/Aem.71.12.8228-8235.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Vazquez-Baeza Y, Gonzalez A, Smarr L, McDonald D, Morton JT, Navas-Molina JA, Knight R (2017) Bringing the dynamic microbiome to life with animations. Cell Host Microbe 21:7–10. https://doi.org/10.1016/j.chom.2016.12.009

    Article  CAS  PubMed  Google Scholar 

  53. Pearson K (1895) Contributions to the mathematical theory of evolution. II. Skew variation in homogenous material. Philos Trans R Soc London 186:343–414

    Article  Google Scholar 

  54. Kendall MG (1938) A new measure of rank correlation. Biometrika 30:81–93. https://doi.org/10.2307/2332226

    Article  Google Scholar 

  55. McCune B, Mefford MJ (2011) PC-ORD: multivariate analysis of ecological data. MjM Software, Gleneden Beach

    Google Scholar 

  56. Berry KJ, Mielke PW (1984) Computation of exact probability values for multi-response permutation procedures (Mrpp). Commun Stat Simul Comput 13:417–432. https://doi.org/10.1080/03610918408812386

    Article  Google Scholar 

  57. McCune B, Grace J, Urban D (2002) Analysis of ecological communities. MjM Software, Gleneden Beach

    Google Scholar 

  58. Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:326–349

    Article  Google Scholar 

  59. Le Bas MJ, Streckeisen AL (1991) The IUGS systematics of ignus rocks. J Geol Soc 148:825–833. https://doi.org/10.1144/gsjgs.148.5.0825

    Article  Google Scholar 

  60. Rades-Rohkohl E, Fränzle O, Hirsch P (1977) Behavior, activities, and effects of bacteria on synthetic quartz monocrystal surfaces. Microb Ecol 4:189–205. https://doi.org/10.1007/bf02015076

    Article  CAS  PubMed  Google Scholar 

  61. Song W, Ogawa N, Takashima-Oguchi C, Hatta T, Matsukura Y (2010) Laboratory experiments on bacterial weathering of granite and its constituent minerals. Biogeomorphology 16:327–336

    Article  Google Scholar 

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Acknowledgments

Sequencing was performed on an Illumina HiSeq2500 purchased with an NSF MRI Grant: DBI-1229361 to WK Thomas. We thank Florencia Fahnestock for assistance in preparing the samples for geochemical study and Michael Rhodes at the University of Massachusetts for assistance acquiring the X-ray fluorescence data.

Funding

This study was funded in part by an award from the University of New Hampshire CoRE program (JB, LST), the University of New Hampshire Summer Teaching Assistant Fellowship (NJE), the University Grants Commission Raman Postdoctoral Fellowship of India (DD), and the College of Life Science and Agriculture at the University of New Hampshire-Durham.

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Authors and Affiliations

  1. Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, 46 College Rd., Durham, NH, 03824-2617, USA

    Nathaniel J. Ennis, Dhanasekaran Dharumaduri & Louis S. Tisa

  2. Department of Microbiology, Bharathidasan University, Tiruchirappalli, Tamil Nadu, India

    Dhanasekaran Dharumaduri

  3. Department of Earth Sciences, University of New Hampshire, Durham, 03824, NH, USA

    Julia G. Bryce

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  1. Nathaniel J. Ennis
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  2. Dhanasekaran Dharumaduri
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  3. Julia G. Bryce
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  4. Louis S. Tisa
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Contributions

NJE, DD, and LST conceived the original idea for the study; NJE, DD, and LST jointly designed the approach and experimental plan; NJE and DD performed the sampling and DNA isolation; NJE prepared the sequenced libraries and analyzed the sequence data; NJE and JB designed the geochemical studies, prepared the samples for analyses, and interpreted and modeled the resulting data; and LST, NJE, JB, and DD wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Louis S. Tisa.

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The authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Electronic Supplementary Material

Figure S1

Photographs of the stones from the sampling locations in Tamil Nadu, India DF- Fort Dindigul; PS- Valikandapuram Sivan Temple, Perambalur; PR- Fort Ranjankudi temple foundation , Perambalur; PRA- Fort Ranjankudi temple wall, Perambalur; TB- Thanjavur Big Temple; TM- Fort Thirumayam, TMA- Fort Thirumayam temple; TF- Fort Tiruchirappalli temple foundation; , TFA- Fort Tiruchirappalli temple wall; PV- Sittanavasal Cave interior; PVA- Sittanavasal Cave exterior. (PDF 306 kb)

Figure S2

Alpha Diversity of Indian Samples Grouped by Stone Type. The Shannon Diversity Index was used to measure alpha diversity of each sample stone type. The diversity of all stone type groupings was not considered significantly different from each other according to the Student’s T test (p > 0.05). (PDF 129 kb)

Figure S3

Major Actinobacteria and Cyanobacteria families in Indian stone microbial communities. Average 16S amplicon data documents the relative abundance of each Actinobacteria (A) and Cyanobacteria (B) family after rarefying. Most Actinobacteria families were present at low abundance in both lithologies, except for Rubrobacteriaceae, which was most prominent in granodiorite. The Cyanobacteria families were generally more prominent in granodiorite, but Nostocaceae was present at low abundance in both lithologies. (PDF 120 kb)

Figure S4

Unweighted Pair Group Method with Arithmetic Mean (UPGMA) Consensus Tree of Indian Stone Microbial Communities. The UPGMA consensus tree was built using the unweighted UniFrac distance matrix of the rarefied feature table. This was done by creating 100 trees from 100 randomly subsampled sequences from each sample. Node labels represent the percentage of the 100 trees that conform to this final consensus configuration. Samples do not clearly cluster by lithology and are color-labeled as granite (red) or granodiorite (blue). (PDF 107 kb)

Table S1

Sampling Climate Data. (PDF 13 kb)

Table S2

Indian Stone Geochemical Analysis. (PDF 17 kb)

Table S3

Summary of Sequencing Data (PDF 8 kb)

Table S4

PCoA Axes Correlations with Environmental Variables. Correlations between PCoA axes and quantitative environmental variables are represented by Pearson’s correlation coefficient (r, r2) and Kendall’s rank correlation (Tau). (PDF 123 kb)

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Ennis, N.J., Dharumaduri, D., Bryce, J.G. et al. Metagenome Across a Geochemical Gradient of Indian Stone Ruins Found at Historic Sites in Tamil Nadu, India. Microb Ecol 81, 385–395 (2021). https://doi.org/10.1007/s00248-020-01598-3

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