Skip to main content
SpringerLink
Log in

Metabolic potential of lithifying cyanobacteria-dominated thrombolitic mats

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Thrombolites are unlaminated carbonate deposits formed by the metabolic activities of microbial mats and can serve as potential models for understanding the molecular mechanisms underlying the formation of lithifying communities. To assess the metabolic complexity of these ecosystems, high throughput DNA sequencing of a thrombolitic mat metagenome was coupled with phenotypic microarray analysis. Functional protein analysis of the thrombolite community metagenome delineated several of the major metabolic pathways that influence carbonate mineralization including cyanobacterial photosynthesis, sulfate reduction, sulfide oxidation, and aerobic heterotrophy. Spatial profiling of metabolite utilization within the thrombolite-forming microbial mats suggested that the top 5 mm contained a more metabolically diverse and active community than the deeper within the mat. This study provides evidence that despite the lack of mineral layering within the clotted thrombolite structure there is a vertical gradient of metabolic activity within the thrombolitic mat community. This metagenomic profiling also serves as a foundation for examining the active role individual functional groups of microbes play in coordinating metabolisms that lead to mineralization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andres MS, Reid RP (2006) Growth morphologies of modern marine stromatolites: a case study from Highborne Cay, Bahamas. Sediment Geol 185(3–4):319–328

    Article  Google Scholar 

  • Andres M, Sumner D, Reid RP, Swart PK (2006) Isotopic fingerprints of microbial respiration in aragonite from Bahamian stromatolites. Geology 34(11):973–976

    Article  CAS  Google Scholar 

  • Arp G, Helms G, Kalinska K, Schumann G, Reimer A, Reitner J, Trichet J (2012) Photosynthesis versus exopolymer degradation in the formation of microbialites on the atoll of Kiritimati, Republic of Kiribati, Central Pacific. Geomicrobiol J 29(1):29–65

    Article  CAS  Google Scholar 

  • Baumgartner LK, Reid RP, Dupraz C, Decho AW, Buckley DH, Spear JR, Przekop KM, Visscher PT (2006) Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sediment Geol 185:131–145

    Article  CAS  Google Scholar 

  • Baumgartner LK, Spear JR, Buckley DH, Pace NR, Reid RP, Visscher PT (2009) Microbial diversity in modern marine stromatolites, Highborne Cay, Bahamas. Environ Microbiol 11(10):2710–2719

    Article  PubMed  Google Scholar 

  • Bhaya D, Grossman AR, Steunou AS, Khuri N, Cohan FM, Hamamura N, Melendrez MC, Bateson MM, Ward DM, Heidelberg JF (2007) Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1(8):703–713

    Article  PubMed  CAS  Google Scholar 

  • Bothe H, Schmitz O, Yates MG, Newton WE (2010) Nitrogen fixation and hydrogen metabolism in cyanobacteria. Microbiol Mol Biol Rev 74(4):529–551

    Article  PubMed  CAS  Google Scholar 

  • Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM, Visscher PT (2007) Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 5(4):401–411

    Article  CAS  Google Scholar 

  • Breitbart M, Hoare A, Nitti A, Siefert J, Haynes M, Dinsdale E, Edwards R, Souza V, Rohwer F, Hollander D (2009) Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Ciénegas, Mexico. Environ Microbiol 11(1):16–34

    Article  PubMed  CAS  Google Scholar 

  • Burns BP, Goh F, Allen M, Neilan BA (2004) Microbial diversity of extant stromatolites in the hypersaline marine environment of Shark Bay, Australia. Environ Microbiol 6(10):1096–1101

    Article  PubMed  CAS  Google Scholar 

  • Burow LC, Woebken D, Marshall IP, Lindquist EA, Bebout BM, Prufert-Bebout L, Hoehler TM, Tringe SG, Pett-Ridge J, Weber PK, Spormann AM, Singer SW (2013) Anoxic carbon flux in photosynthetic microbial mats as revealed by metatranscriptomics. ISME J 7(4):817–829

    Article  PubMed  CAS  Google Scholar 

  • Couradeau E, Benzerara K, Moreira D, Gerard E, Kazmierczak J, Tavera R, Lopez-Garcia P (2011) Prokaryotic and eukaryotic community structure in field and cultured microbialites from the alkaline Lake Alchichica (Mexico). PLoS One 6(12):e28767

    Article  PubMed  CAS  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform 11:485

    Article  Google Scholar 

  • Decho AW (1990) Microbial exopolymer secretions in ocean environments - their role(s) in food webs and marine processes. Oceanogr Mar Biol 28:73–153

    Google Scholar 

  • Decho AW (2000) Microbial biofilms in intertidal systems: an overview. Cont Shelf Res 20:1257–1273

    Article  Google Scholar 

  • Desnues CG, Rodriguez-Brito B, Rayhawk S, Kelley S, Tran T, Haynes M, Lui H, Hall D, Angly FE, Edwards RA, Thurber RV, Reid RP, Siefert J, Souza V, Valentine D, Swan B, Breitbart M, Rohwer F (2008) Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452:340–345

    Article  PubMed  CAS  Google Scholar 

  • Dinsdale EA, Edwards RA, Bailey BA, Tuba I, Akhter S, McNair K, Schmieder R, Apkarian N, Creek M, Guan E, Hernandez M, Isaacs K, Peterson C, Regh T, Ponomarenko V (2013) Multivariate analysis of functional metagenomes. FGENE 4:41

    CAS  Google Scholar 

  • Dupraz C, Visscher PT (2005) Microbial lithification in marine stromatolites and hypersaline mats. Trends in Microbiol 13(9):429–438

    Article  CAS  Google Scholar 

  • Dupraz C, Reid RP, Braissant O, Decho AW, Norman RS, Visscher PT (2009) Processes of carbonate precipitation in modern microbial mats. Earth Sci Rev 96(3):141–162

    Article  CAS  Google Scholar 

  • Edgcomb VP, Bernhard JM, Beaudoin D, Pruss S, Welander PV, Schubotz F, Mehay S, Gillespie AL, Summons RE (2013) Molecular indicators of microbial diversity in oolitic sands of Highborne Cay, Bahamas. Geobiology 11(3):234–251

    Article  PubMed  CAS  Google Scholar 

  • Faria JC, Demetrio CGB (2008) BPCA: bioplot of multivariate data based on principal components analysis. R package version 1.02 edn. UESC and ESALQ, Ilheus, Bahia, Brasil and Piracicaba, Sao Paulo, Brasil

  • Feist AM, Scholten JCM, Palsson BO, Brockman FJ, Ideker T (2006) Modeling methanogenesis with a genome-scale metabolic reconstruction of Methanosarcina barkeri. Mol Syst Biol 2:2006.0004

    Google Scholar 

  • Foster JS, Green SJ (2011) Microbial diversity in modern stromatolites. In: Seckbach J, Tewari V (eds) Cellular origin, life in extreme habitats and astrobiology: interactions with sediments. Springer, Berlin, pp 385–405

    Google Scholar 

  • Gallagher KL, Braissant O, Kading TJ, Dupraz C, Visscher PT (2013) Phosphate-related artifacts in carbonate mineralization experiments. J Sediment Res 83(1):37–49

    Article  Google Scholar 

  • Goh F, Allen MA, Leuko S, Kawaguchi T, Decho AW, Burns BP, Neilan BA (2009) Determining the specific microbial populations and their spatial distribution within the stromatolite ecosystem of Shark Bay. ISME J 3:383–396

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Alvarez V, Teal TK, Schmidt TM (2009) Systematic artifacts in metagenomes from complex microbial communities. ISME J 3(11):1314–1317

    Article  PubMed  Google Scholar 

  • Grotzinger JP, Knoll AH (1999) Stromatolites in Precambrian carbonates: evolutionary mileposts or environmental dipsticks? Annu Rev Earth Planet Sci 27:313–358

    Article  PubMed  CAS  Google Scholar 

  • Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17(3):377–386

    Article  PubMed  CAS  Google Scholar 

  • Kawaguchi T, Decho AW (2000) Biochemical characterization of cyanobacterial extracellular polymers (EPS) from modern marine stromatolites (Bahamas). Prep Biochem Biotech 30(4):321–330

    Article  CAS  Google Scholar 

  • Khodadad CL, Foster JS (2012) Metagenomic and metabolic profiling of nonlithifying and lithifying stromatolitic mats of Highborne Cay, The Bahamas. PLOS One 7(5):e38229

    Article  PubMed  CAS  Google Scholar 

  • Kolde R (2013) pheatmap: Pretty Heatmaps. version 0.7.4 edn. R package

  • Kunin V, Raes J, Harris JK, Spear JR, Walker JJ, Ivanova N, von Mering C, Bebout BM, Pace NR, Bork P, Hugenholtz P (2008) Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol Syst Biol 4:198

    Article  PubMed  Google Scholar 

  • Leuko S, Goh F, Allen MA, Burns BP, Walter MR, Neilan BA (2007) Analysis of intergenic spacer region length polymorphisms to investigate the halophilic archaeal diversity of stromatolites and microbial mats. Extremophiles 11(1):203–210

    Article  PubMed  CAS  Google Scholar 

  • Liaw A, Weiner M (2002) Classification and regression by randomforest. R News 2(3):18–22

    Google Scholar 

  • Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35(18):e120

    Article  PubMed  Google Scholar 

  • Macintyre IG, Prufert-Bebout L, Reid RP (2000) The role of endolithic cyanobacteria in the formation of lithified lamiae in Bahamian stromatolites. Sedimentology 47:915–921

    Article  Google Scholar 

  • Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9:386

    Article  CAS  Google Scholar 

  • Mobberley JM, Ortega MC, Foster JS (2012) Comparative microbial diversity analyses of modern marine thrombolitic mats by barcoded pyrosequencing. Environ Microbiol 14:82–100

    Article  PubMed  CAS  Google Scholar 

  • Myshrall K, Mobberley JM, Green SJ, Visscher PT, Havemann SA, Reid RP, Foster JS (2010) Biogeochemical cycling and microbial diversity in the modern marine thrombolites of Highborne Cay, Bahamas. Geobiology 8:337–354

    Article  PubMed  CAS  Google Scholar 

  • Nitti A, Daniels CA, Siefert J, Souza V, Hollander D, Breitbart M (2012) Spatially resolved genomic, stable isotopic, and lipid analyses of a modern freshwater microbialite from Cuatro Cienegas, Mexico. Astrobiology 12(7):685–698

    Article  PubMed  CAS  Google Scholar 

  • Paerl HW, Steppe TF, Reid RP (2001) Bacterially mediated precipitation in marine stromatolites. Environ Microbiol 3(2):123–130

    Article  PubMed  CAS  Google Scholar 

  • Peimbert M, Alcaraz LD, Bonilla-Rosso G, Olmedo-Alvarez G, Garcia-Oliva F, Segovia L, Eguiarte LE, Souza V (2012) Comparative metagenomics of two microbial mats at Cuatro Ciénegas Basin I: ancient lessons on how to cope with an environment under severe nutrient stress. Astrobiology 12(7):648–658

    Article  PubMed  CAS  Google Scholar 

  • Peters JW, Boyd ES, D’Adamo S, Mulder DW, Posewitz MC (2013) Hydrogenases, nitrogenases, anoxia, and H2 production in water-oxidizing phototrophs. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy developments in applied phycology, vol 5. Springer, Dordrecht, pp 37–75

    Chapter  Google Scholar 

  • Pinckney J, Paerl HW, Reid RP, Bebout BM (1995) Ecophysiology of stromatolitic microbial mats, Lee Stocking Island, Exuma Cays, Bahamas. Microb Ecol 29:19–37

    Article  PubMed  CAS  Google Scholar 

  • Planavsky N, Ginsburg RN (2009) Taphonomy of modern marine Bahamian microbialites. Palaios 24:5–17

    Article  Google Scholar 

  • Planavsky N, Reid RP, Andres M, Visscher PT, Myshrall KL, Lyons TW (2009) Formation and diagenesis of modern marine calcified cyanobacteria. Geobiology 7:566–576

    Article  PubMed  CAS  Google Scholar 

  • Reid RP, Visscher PT, Decho AW, Stolz JF, Bebout BM, Dupraz C, Macintyre IG, Paerl HW, Pinckney JL, Prufert-Bebout L, Steppe TF, DesMarais DJ (2000) The role of microbes in accretion, lamination and early lithification of modern marine stromatolites. Nature 406(6799):989–992

    Article  PubMed  CAS  Google Scholar 

  • Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers YH, Falcon LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5(3):e77

    Article  PubMed  Google Scholar 

  • Santos F, Pena A, Nogales B, Soria–Soria E, Del Cura MA, Gonzalez-Martin JA, Anton J (2010) Bacterial diversity in dry modern freshwater stromatolites from Ruidera Pools Natural Park, Spain. Syst Appl Microbiol 33(4):209–221

    Article  PubMed  CAS  Google Scholar 

  • Steppe TF, Pinckney JL, Dyble J, Paerl HW (2001) Diazotrophy in modern marine Bahamian stromatolites. Microb Ecol 41(1):36–44

    PubMed  CAS  Google Scholar 

  • Steven B, Gellegos-Graves L, Starkenburg SR, Chain PS, Kuske CR (2012) Targeted and shotgun metagenomic approaches provide different descriptions of dryland soil microbial communities in a manipulated field study. Environ Microbiol Rep 4(2):249–256

    Article  Google Scholar 

  • R Development Core Team (2010) A language and environment for statistical computing. 3-900051-07-0 edn. R Foundation for Statistical Computing, Vienna, Austria

  • van der Meer MT, Schouten S, Damste JS, Ward DM (2007) Impact of carbon metabolism on 13C signatures of cyanobacteria and green non-sulfur-like bacteria inhabiting a microbial mat from an alkaline siliceous hot spring in Yellowstone National Park (USA). Environ Microbiol 9(2):482–491

    Article  PubMed  Google Scholar 

  • Visscher PT, Stolz JF (2005) Microbial mats as bioreactors: populations, processes and products. Palaeogeogr Palaeoclimatol Palaeoecol 219:87–100

    Article  Google Scholar 

  • Visscher PT, Reid RP, Bebout BM, Hoeft SE, Macintyre IG, Thompson JA (1998) Formation of lithified micritic laminae in modern marine stromatolites (Bahamas): the role of sulfur cycling. Amer Mineral 83:1482–1493

    CAS  Google Scholar 

  • Visscher PT, Reid RP, Bebout BM (2000) Microscale observations of sulfate reduction: correlation of microbial activity with lithified micritic laminae in modern marine stromatolites. Geology 28(10):919–922

    Article  CAS  Google Scholar 

  • Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PS, Chan PP, Gollabgir A, Hemp J, Hugler M, Karr EA, Konneke M, Shin M, Lawton TJ, Lowe T, Martens-Habbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107(19):8818–8823

    Article  PubMed  CAS  Google Scholar 

  • Wilke A, Harrison T, Wilkening J, Field D, Glass EM, Kyrpides N, Mavrommatis K, Meyer F (2012) The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools. BMC Bioinform 13:141

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Louis Sherman and Pramod Wangikar for organizing the first Indo-US workshop on Cyanobacteria: Molecular Networks to Biofuels, which led to this manuscript. The research was supported by the NASA: Exobiology and Evolutionary Biology Program Element (NNX12AD64G) awarded to Jamie S. Foster. Jennifer M. Mobberley was supported by a NASA Graduate Student Research Program fellowship (NNX10AO18H).

Author information

Authors and Affiliations

  1. Department of Microbiology and Cell Science, University of Florida, Space Life Sciences Lab, Kennedy Space Center, FL, 32899, USA

    Jennifer M. Mobberley, Christina L. M. Khodadad & Jamie S. Foster

Authors
  1. Jennifer M. Mobberley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christina L. M. Khodadad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jamie S. Foster
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jamie S. Foster.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mobberley, J.M., Khodadad, C.L.M. & Foster, J.S. Metabolic potential of lithifying cyanobacteria-dominated thrombolitic mats. Photosynth Res 118, 125–140 (2013). https://doi.org/10.1007/s11120-013-9890-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9890-6

Keywords

Search

Navigation