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Comparison of Rock Varnish Bacterial Communities with Surrounding Non-Varnished Rock Surfaces: Taxon-Specific Analysis and Morphological Description

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Abstract

Rock varnish is a thin layer of Fe and Mn oxyhydroxides with embedded clay minerals that contain an increased Mn/Fe ratio compared to that of the Earth’s crust. Even if the study of rock varnish has important implications in several fields, the composition of epilithic bacterial communities and the distribution of taxa on varnish surfaces are still not wholly described. The aim of this study was (i) to identify the bacterial taxa which show the greatest variation between varnish and non-varnish environments, collected from the same rock, and (ii) to describe the morphology of epilithic communities through scanning electron microscopy (SEM). Triplicate samples of rock surfaces with varnish and triplicate samples without varnish were collected from five sites in Matsch Valley (South Tyrol, Italy). The V4 region of 16S rRNA gene was analyzed by Illumina sequencing. Fifty-five ubiquitous taxa have been examined to assess variation between varnish and non-varnish. Cyanobacteria, Chloroflexi, Proteobacteria along with minor taxa such as Solirubrobacterales, Conexibaxter, and Rhodopila showed significant variations of abundance, diversity, or both responding to the ecology (presence/absence of varnish). Other taxa, such as the genus Edaphobacter, showed a more marked spatial variation responding to the sampling site. SEM images showed a multitude of bacterial morphologies and structures involved in the process of attachment and creation of a suitable environment for growth. The features emerging from this analysis suggest that the highly oxidative Fe and Mn-rich varnish environment favors anoxigenic autotrophy and establishment of highly specialized bacteria.

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References

  1. Dorn R (2007) Rock varnish. Geochemical sediments and landscapes. Wiley Online Library, pp 246–297

  2. Liu T, Broecker WS (2000) How fast does rock varnish grow? Geology 28:183–186

    Article  CAS  Google Scholar 

  3. Engel CG, Sharp RP (1958) Chemical data on desert varnish. Geol Soc Am Bull 69:487–518

    Article  CAS  Google Scholar 

  4. Krinsley D, Dorn RI, DiGregorio B (2009) Astrobiological implications of rock varnish in Tibet. Astrobiology 9:551–562

    Article  CAS  PubMed  Google Scholar 

  5. Northup DE, Snider JR, Spilde MN et al (2010) Diversity of rock varnish bacterial communities from Black Canyon, New Mexico. J Geophys Res-Biogeo 115:1–19

    Article  Google Scholar 

  6. Liu T, Broecker WS, Stein M (2013) Rock varnish evidence for a younger Dryas wet period in the Dead Sea Basin. Geophys Res Lett 40:2229–2235

    Article  Google Scholar 

  7. Eggleston CM, Parkinson BA (2012) Natural solar cells on Earth and Mars. Goldshmidt Conf Abstr 1678

  8. Hooke RL, Yang H-Y, Weiblen PW (1969) Desert varnish: an electron probe study. J Geol 77:275–288

    Article  CAS  Google Scholar 

  9. Allen CC, Probst LW, Flood BE et al (2004) Meridiani Planum hematite deposit and the search for evidence of life on Mars—Iron mineralization of microorganisms in rock varnish. Icarus 171:20–30

    Article  CAS  Google Scholar 

  10. Perry RS, Kolb VM (2004) Biological and organic constituents of desert varnish: review and new hypotheses. Opt Sci Technol SPIE’s 48th Annu Meet pp 202–217

  11. Mergelov NS, Goryachkin SV, Shorkunov IG et al (2012) Endolithic pedogenesis and rock varnish on massive crystalline rocks in East Antarctica. Eurasian Soil Sci 45:901–917

    Article  CAS  Google Scholar 

  12. Weber KA, Achenbach LA, Coates JD (2006) Microbes pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764

    Article  CAS  PubMed  Google Scholar 

  13. Tebo BM, Johnson HA, McCarthy JK, Templeton AS (2005) Geomicrobiology of manganese(II) oxidation. Trends Microbiol 13:421–428

    Article  CAS  PubMed  Google Scholar 

  14. Learman DR, Voelker BM, Vazquez-Rodriguez AI, Hansel CM (2011) Formation of manganese oxides by bacterially generated superoxide. Nat Geosci 4:95–98

    Article  CAS  Google Scholar 

  15. Krumbein WE, Jens K (1981) Biogenic rock varnishes of the Negev Desert (Israel) an ecological study of iron and manganese transformation by cyanobacteria and fungi. Oecologia 50:25–38

    Article  Google Scholar 

  16. Kuhlman KR, Fusco WG, La Duc MT et al (2006) Diversity of microorganisms within rock varnish in the Whipple Mountains, California. Appl Environ Microbiol 72:1708–1715

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Krinsley DH, Dorn RI, DiGregorio BE et al (2012) Rock varnish in New York: an accelerated snapshot of accretionary processes. Geomorphology 138:339–351

    Article  Google Scholar 

  18. Penna D, Engel M, Mao L et al (2014) Tracer-based analysis of spatial and temporal variation of water sources in a glacierized catchment. Hydrol Earth Syst Sci Discuss 11:4879–4924

    Article  Google Scholar 

  19. Habler G, Thöni M, Grasemann B (2009) Cretaceous metamorphism in the Austroalpine Matsch Unit (Eastern Alps): the interrelation between deformation and chemical equilibration processes. Mineral Petrol 97:149–171

    Article  CAS  Google Scholar 

  20. Knoll C, Kerschner H (2010) A glacier inventory for South Tyrol, Italy, based on airborne laser-scanner data. Ann Glaciol 50:46–52

    Article  Google Scholar 

  21. Feinstein LM, Sul WJ, Blackwood CB (2009) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol 75:5428–5433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Lane DS, Stackebrandt E, Goodfellow M (1990) 16S and 23S rRNA sequencing. In: Stackebrandt E and Goodfellow M (ed) Nucleic Acid Tech Bact Syst NY, John Wiley and Sons, pp 115–175

  23. Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Echlin P (2009) Handbook of sample preparation for scanning electron microscopy and X-ray microanalysis. Springer

  25. Aronesty E (2013) Comparison of sequencing utility programs. TOBIOIJ 7:1–8

    Article  Google Scholar 

  26. Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  CAS  PubMed  Google Scholar 

  28. R Core Team (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/

  29. Cole JR, Wang Q, Cardenas E et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490

    Article  PubMed Central  PubMed  Google Scholar 

  33. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Parchert KJ, Spilde MN, Porras-Alfaro A et al (2012) Fungal communities associated with rock varnish in Black Canyon, New Mexico: casual inhabitants or essential partners? Geomicrobiol J 29:752–766

    Article  CAS  Google Scholar 

  35. Marnocha CL, Dixon JC (2013) Bacterially facilitated rock-coating formation as a component of the geochemical budget in cold climates: an example from Kärkevagge, Swedish Lapland. Geomorphology 218:41–51

    Google Scholar 

  36. Claesson MJ, Wang Q, O’Sullivan O et al (2010) Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Res 38:e200

    Article  PubMed Central  PubMed  Google Scholar 

  37. Yabe S, Aiba Y, Sakai Y et al (2011) Thermogemmatispora onikobensis gen. nov., sp. nov. and Thermogemmatispora foliorum sp. nov., isolated from fallen leaves on geothermal soils, and description of Thermogemmatisporaceae fam. nov. and Thermogemmatisporales. Int J Syst Evol Microbiol 61:903–910

    Article  CAS  PubMed  Google Scholar 

  38. Jones RT, Robeson MS, Lauber CL et al (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Catão ECP, Lopes FAC, Araújo JF et al (2014) Soil Acidobacterial 16S rRNA gene sequences reveal subgroup level differences between Savanna-Like Cerrado and Atlantic Forest Brazilian biomes. Int J Microbiol 2014:156341

    Article  PubMed Central  PubMed  Google Scholar 

  40. Kuhlman KR, Venkat P, La Duc MT et al (2008) Evidence of a microbial community associated with rock varnish at Yungay, Atacama Desert, Chile. J Geophys Res 113:G04022

    Google Scholar 

  41. Gupta RS, Chander P, George S (2013) Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexi class. nov. into the suborder Chloroflexineae subord. nov., consisting of the emended family Oscillochlorida. Antonie Van Leeuwenhoek 103:99–119

    Article  PubMed  Google Scholar 

  42. Benning MM, Meyer TE, Holden HM (1996) Molecular structure of a high potential cytochrome c2 isolated from Rhodopila globiformis. Arch Biochem Biophys 333:338–348

    Article  CAS  PubMed  Google Scholar 

  43. Taylor-George S, Palmer F, Staley JT et al (1983) Fungi and bacteria involved in desert varnish formation. Microb Ecol 9:227–245

    Article  CAS  PubMed  Google Scholar 

  44. Ehrlich HL, Newman DK (2008) Geomicrobiology, 5th edn. CRC Press, Boca Raton, 656 p

    Book  Google Scholar 

  45. Jiao Y, Kappler A, Croal LR, Johnson DB (2005) Isolation and characterization of a genetically tractable photoautotrophic Fe(II)-oxidizing bacterium, Rhodopseudomonas palustris strain TIE-1. Appl Environ Microbiol 71(8):4487–4496

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Caccavo FJ, Das A (2002) Adhesion of dissimilatory Fe(III)-reducing bacteria to Fe(III) minerals. Geomicrobiol J 19:161–177

    Article  CAS  Google Scholar 

  47. Roberts JA (2004) Inhibition and enhancement of microbial surface colonization: the role of silicate composition. Chem Geol 212:313–327

    Article  CAS  Google Scholar 

  48. Gruszczynski M, Kowalski B, Soltysik R, Hercman H (2004) Tectonic origin of the unique Holocene travertine from the Holy Cross Mts.: microbially and abiologically mediated calcium carbonate, and manganese oxide precipitation. Acta Geol Pol 54:61–76

    Google Scholar 

  49. Wang X, Zeng L, Wiens M et al (2011) Evidence for a biogenic, microorganismal origin of rock varnish from the Gangdese Belt of Tibet. Micron 42:401–411

    Article  CAS  PubMed  Google Scholar 

  50. Ivarsson M, Holmström S (2012) The use of ESEM in geobiology, scanning electron microscopy, Dr Viacheslav Kazmiruk (Ed), ISBN: 978-953-51-0092-8, InTech

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Acknowledgments

We acknowledge the help of Kjell Jansson for his suggestions for SEM analysis, Boyke Bunk for bioinformatics, and Anders Andersson for his help in statistics. The present study was supported by the Erich-Ritter and the Herzog-Sellenberg Foundations within the Stifterverband für die Deutsche Wissenschaft within the EMERGE project (CUP I41J11000490007), and the grants from Liljevalchs fund, Stockholm University. English quality was edited by Dr. James Haile and Hilderd Crill.

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Correspondence to Lorenzo Brusetti.

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Fig. SM1

Shannon (upper row) and Chao (lower row) diversity indices for Cyanobacteria, Solirubrobacterales and Conexibacter, and table with diversity indices values for each of the sites. (PPT 150 kb)

Fig. SM2

Bacterial community profile based on Illumina sequencing (on average 354494 reads per sample). Major (> 99.9 % of the reads) phyla, classes and orders are depicted. The table in the lower right quarter of the picture is a list of the other taxa divided according to their occurrence in one of the two environment or in both; the number of samples in which the taxa occur are given in the parenthesis. (PPT 385 kb)

Fig. SM3

Interactions between microbes and minerals: (A) structure analogous to figure 3G; with stone surface corrosion by filamentous bacteria from site 3 varnish; (B) filamentous forms colonizing a microfracture from non-varnish of site 4; (C) unknown structures from varnish of site 5; (D) unknown blood-cell like shapes from non-varnish of site 2; (E) cave buds of unknown origin from non-varnish sample of site 3; (F) putative rock-dwelling microcolonial fungi, from varnish of site 5; (G) analogous structure as in (F) plus enlargements of the biological structure (H-I) from varnish of site 3. (PPT 2333 kb)

Fig. SM4

Landscape pictures, extracellular structure and dividing cells: (A) micrometre thick coating on mineral surface from varnish of site 4; (B) landscape aspect of non-varnish samples of site 4; (C) filamentous form from varnish of site 3; (D) tetra-cocci with external slime from varnish of site 2; (E) coccal shape with external biofilms from varnish of site 3 and (F) varnish site 2; (G) coccal shapes adhering to the mineral surface, zoom from figure 2c; (H) reproducing bacteria from varnish of site 3 and (I) non-varnish of site 2. (PPT 2050 kb)

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Esposito, A., Ahmed, E., Ciccazzo, S. et al. Comparison of Rock Varnish Bacterial Communities with Surrounding Non-Varnished Rock Surfaces: Taxon-Specific Analysis and Morphological Description. Microb Ecol 70, 741–750 (2015). https://doi.org/10.1007/s00248-015-0617-4

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