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Vertical Distribution of Functional Potential and Active Microbial Communities in Meromictic Lake Kivu

  • Microbiology of Aquatic Systems
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Abstract

The microbial community composition in meromictic Lake Kivu, with one of the largest CH4 reservoirs, was studied using 16S rDNA and ribosomal RNA (rRNA) pyrosequencing during the dry and rainy seasons. Highly abundant taxa were shared in a high percentage between bulk (DNA-based) and active (RNA-based) bacterial communities, whereas a high proportion of rare species was detected only in either an active or bulk community, indicating the existence of a potentially active rare biosphere and the possible underestimation of diversity detected when using only one nucleic acid pool. Most taxa identified as generalists were abundant, and those identified as specialists were more likely to be rare in the bulk community. The overall number of environmental parameters that could explain the variation was higher for abundant taxa in comparison to rare taxa. Clustering analysis based on operational taxonomic units (OTUs at 0.03 cutoff) level revealed significant and systematic microbial community composition shifts with depth. In the oxic zone, Actinobacteria were found highly dominant in the bulk community but not in the metabolically active community. In the oxic–anoxic transition zone, highly abundant potentially active Nitrospira and Methylococcales were observed. The co-occurrence of potentially active sulfur-oxidizing and sulfate-reducing bacteria in the anoxic zone may suggest the presence of an active yet cryptic sulfur cycle.

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References

  1. Casamayor EO, Llirós M, Picazo A, Barberán CM, Borrego CM, Camacho A (2012) Contribution of deep dark fixation processes to overall CO2 incorporation and large vertical changes of microbial populations in stratified karstic lakes. Aquat Sci 74(1):61–75

    Article  CAS  Google Scholar 

  2. Eiler A, Heinrich F, Bertilsson S (2012) Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J 6:330–342

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Lehours AC, Bardot C, Thenot A, Debroas D, Fonty G (2005) Anaerobic microbial communities in Lake Pavin, a unique meromictic lake in France. Appl Environ Microbiol 71:7389–7400

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Logue JB, Lindström ES (2010) Species sorting affects bacterioplankton community composition as determined by 16S rDNA and 16S rRNA fingerprints. ISME J 4:729–738

    Article  CAS  PubMed  Google Scholar 

  5. Van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S et al (2007) The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. Proc Natl Acad Sci USA 104:20404–20409

    Article  PubMed Central  PubMed  Google Scholar 

  6. Lennon JJ, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev 9:119–130

    CAS  Google Scholar 

  7. Huber JA, Welch DBM, Morrison HG, Huse SM, Neal PR, Butterfield DA, Sogin ML (2007) Microbial population structures in the deep marine biosphere. Science 318:97–100

    Article  CAS  PubMed  Google Scholar 

  8. Huber JA, Cantin HV, Huse SM, Mark Welch DB, Sogin ML, Butterfield DA (2010) Isolated communities of Epsilonproteobacteria in hydrothermal vent fluids of the Mariana Arc sea mounts. FEMS Microbiol Ecol 73:538–549

    CAS  PubMed  Google Scholar 

  9. Sogin ML, Morrison HG, Huber JA et al (2006) Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc Natl Acad Sci USA 103:12115–12120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Pedrós-Alió C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14:257–263

    Article  PubMed  Google Scholar 

  11. Polymenakou PN, Lampadariou N, Mandalakis M, Tselepides A (2009) Phylogenetic diversity of sediment bacteria from the southern Cretan margin, Eastern Mediterranean Sea. Syst Appl Microbiol 32:17–26

    Article  CAS  PubMed  Google Scholar 

  12. Lanzén A, Jørgensen SL, Bengtsson MM, Jonassen I, Øvreås L, Urich T (2011) Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA. FEMS Microbiol Ecol 77:577–589

    Article  PubMed  Google Scholar 

  13. Campbell BJ, Yu L, Heidelberg JF, Kirchman DL (2011) Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci USA 108:12776–12781

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Campbell BJ, Kirchman DL (2013) Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J 7:210–220

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci USA 107:5881–5886

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Moeseneder MM, Arrieta JM, Herndl GJ (2005) A comparison of DNA- and RNA-based clone libraries from the same marine bacterioplankton community. FEMS Microbiol Ecol 51(3):341–52

    Article  CAS  PubMed  Google Scholar 

  17. Schmid M, Halbwachs M, Wehrli B, Wüest A (2005) Weak mixing in Lake Kivu: new insights indicate increasing risk of uncontrolled gas eruption. Geochem Geophys Geosyst 6, Q07009

    Article  Google Scholar 

  18. Borges AV, Abril G, Delille B, Descy JP, Darchambeau F (2011) Diffusive methane emissions to the atmosphere from Lake Kivu (Eastern Africa). J Geophys Res 116, G03032

    Google Scholar 

  19. Pasche N, Schmid M, Vasquez F, Schubert CJ, Wüest A, Kessler JD, Pack MA, Reeburgh WS, Bürgmann H (2011) Methane sources and sinks in Lake Kivu. J Geophys Res 116, G03006

    Google Scholar 

  20. İnceoğlu Ö, Llirós M, Garcia-Armisen T, Crowe SA, Michiels C, Darchambeau F, Descy JP, Servais P Distribution of bacteria and archaea in meromictic tropical Lake Kivu (Africa). Aquat Microb Ecol. doi:10.3354/ame01737. In press.

  21. Llirós M, Gich F, Plasencia A, Auguet JC, Darchambeau F, Casamayor EO, Descy JP, Borrego C (2010) Vertical distribution of ammonia-oxidizing Crenarchaeota and methanogens in the epipelagic waters of Lake Kivu (Rwanda-Democratic Republic of the Congo). Appl Environ Microbiol 76(20):6853–6863

    Article  PubMed Central  PubMed  Google Scholar 

  22. Darchambeau F, Sarmento H, Descy J-P (2014) Primary production in a tropical large lake: the role of phytoplankton composition. Sci Total Environ 473–474:178–188

    Article  PubMed  Google Scholar 

  23. Sarmento H, Isumbisho M, Descy JP (2006) Phytoplankton ecology of Lake Kivu. J Plankton Res 28:815–829

    Article  CAS  Google Scholar 

  24. Isumbisho M, Sarmento H, Kaningini B, Micha JC, Descy JP (2006) Zooplankton of Lake Kivu, East Africa, half a century after the Tanganyika sardine introduction. J Plankton Res 28:971–989

    Article  Google Scholar 

  25. Schmid M, Wüest A (2012) In: Descy JP, Darchambeau F, Schmid M (eds) Stratification mixing and transport processes in Lake Kivu. Springer, Lake Kivu, pp 13–30

    Google Scholar 

  26. Wright JJ, Konwar KM, Hallam SJ (2012) Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol 10(6):381–394

    CAS  PubMed  Google Scholar 

  27. Standing Committee of Analysts (1981) Methods for the examination of waters and associated materials Ammonia in waters. HMSO, London

    Google Scholar 

  28. EatonE, Archie AE, Rice EW, Clesce LS (2012) Standard Methods for the Examination of Water Wastewater, APHA 22nd Edition

  29. Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5(1):62–71

    Article  CAS  PubMed  Google Scholar 

  30. Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458

    Article  CAS  Google Scholar 

  31. Llirós M, Casamayor E, Borrego CM (2008) High archaeal richness in the water column of a freshwater sulfurous karstic lake along an inter-annual study. FEMS Microbiol Ecol 66:331–342

    Article  PubMed  Google Scholar 

  32. Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW, Delong EF (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105:3805–10

  33. Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65(11):5066–5073

    PubMed Central  CAS  PubMed  Google Scholar 

  34. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148:3521–3530

    Article  CAS  PubMed  Google Scholar 

  35. Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and ı genes in soils. Appl Environ Microbiol 72(8):5181–5189

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Development Core Team R (2011) R: A language and environment for statistical computing R Foundation for Statistical Computing. Austria, Vienna, Available at: http://www.R-project.org

    Google Scholar 

  37. Callaway TR, Dowd SE, Wolcott RD, Sun Y, McReynolds JL et al (2009) Evaluation of the bacterial diversity in cecal contents of laying hens fed various molting diets by using bacterial tag encoded FLX amplicon pyrosequencing. Poult Sci 88:298–302

    Article  CAS  PubMed  Google Scholar 

  38. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E, Rhoads D (2008) Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One 3, e3326

    Article  PubMed Central  PubMed  Google Scholar 

  39. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27(16):2194–2200

    Article  CAS  Google Scholar 

  40. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M 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 

  41. Clarke KR, Gorley RN (2006) PRIMER V6: usermanual/Tutorial Plymouth. PRIMER-E, UK

    Google Scholar 

  42. Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton

    Google Scholar 

  43. Logares R, Lindström ES, Langenheder S, Logue JB, Paterson H, Laybourn-Parry J, Rengefors K, Tranvik L, Bertilsson S (2013) Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J 7(5):937–48

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers G, Raes J, Huttenhower C (2012) Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8(7), e1002606

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T, Warnecke F, Sommaruga R, Sekar R, Hofer JS, Pernthaler J (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2503

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation comparison of fractions. Ecology 87:2614–2625

    Article  PubMed  Google Scholar 

  47. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL (2012) vegan: Community Ecology Package R package version 20-5 http://CRAN.R-project.org/package=vegan

  48. Dimitriu PA, Pinkart HC, Peyton BM, Mormile MR (2008) Spatial and temporal patterns in the microbial diversity of a meromictic soda lake in Washington State. Appl Environ Microbiol 74:4877–4888

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Koizumi Y, Kojima H, Oguri K, Kitazato H, Fukui M (2004) Vertical and temporal shifts in microbial communities in the water column and sediment of saline meromictic Lake Kaiike (Japan), as determined by a 16S rDNA-based analysis, and related to physicochemical gradients. Environ Microbiol 6:622–637

    Article  CAS  PubMed  Google Scholar 

  50. Lentini V, Gugliandolo C, Maugeri TL (2012) Vertical distribution of Archaea and Bacteria in a meromictic lake as determined by fluorescent in situ hybridization. Curr Microbiol 64:66–74

    Article  CAS  PubMed  Google Scholar 

  51. Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75(1):14–49

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Kolmonen E, Sivonen K, Rapala J, Haukka K (2004) Diversity of Cyanobacteria and heterotrophic bacteria in cyanobacterial blooms in Lake Joutikas, Finland. Aquat Microb Ecol 36:201–211

    Article  Google Scholar 

  53. Hahn MW, Lünsdorf H, Wu Q, Schauer M, Höfle MG, Boenigk J, Stadler P (2003) Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Appl Environ Microbiol 69:1442–1451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. Kemp PF, Lee S, LaRoche J (1993) Estimating the growth rate of slowly growing marine bacteria from RNA content. Appl Environ Microbiol 59:2594–2601

    PubMed Central  CAS  PubMed  Google Scholar 

  55. Pernthaler J, Posch T, Simek K, Vrba J, Pernthaler A, Glöckner FO, Nübel U, Psenner R, Amann R (2001) Predator-specific enrichment of actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture. Appl Environ Microbiol 67:2145–2155

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  56. Brümmer IHM, Felske ADM, Wagner-Döbler I (2004) Diversity and seasonal changes of uncultured Planctomycetales in river biofilms. Appl Environ Microbiol 70:5094–5101

    Article  PubMed Central  PubMed  Google Scholar 

  57. Mary I, Cummings DG, Biegala IC, Burkill PH, Archer SD, Zubkov MV (2006) Seasonal dynamics of bacterioplankton community structure ata coastal station in the western English Channel. Aquat Microb Ecol 41:119–126

    Article  Google Scholar 

  58. Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol Ò, Malits A, Marrasé C (2004) Changes in bacterioplankton composition under different phyto-plankton regimens. Appl Environ Microbiol 70:6753

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Pizzetti I, Fuchs BM, Gerdts G, Wichels A, Wiltshire KH, Amann R (2011) Temporal variability of coastal Planctomycetes clades at Kabeltonne station, North Sea. Appl Environ Microbiol 77:5009–5017

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  60. Tadonléké RD (2007) Strong coupling between natural Planctomycetes and changes in the quality of dissolved organic matter in freshwater samples. FEMS Microbiol Ecol 59:543–555

    Article  PubMed  Google Scholar 

  61. Bauer M, Kube M, Teeling H, Richter M, Lombardot T, Allers E, Würdemann CA, Quast C, Kuhl H, Knaust F, Woebken D, Bischof K, Mussmann M, Choudhuri JV, Meyer F, Reinhardt R, Amann RI, Glöckner FO (2006) Whole genome analysis of the marine Bacteroidetes ‘Gramellaforsetii’ reveals adaptations to degradation of polymeric organic matter. Environ Microbiol 8:2201–2213

    Article  CAS  PubMed  Google Scholar 

  62. DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934

    Article  Google Scholar 

  63. Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T (2005) Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7:860–873

    Article  CAS  PubMed  Google Scholar 

  64. Morana C, Sarmento H, Descy JP, Gasol JM, Borges AV, Bouillon S, Darchambeau F (2014) Production of dissolved organic matter by phytoplankton and its uptake by heterotrophic prokaryotes in large tropical lakes. Limnol Oceanogr 59(4):1364–1375

    Article  CAS  Google Scholar 

  65. Elshahed MS, Youssef NH, Luo Q, Najar FZ, Roe BA, Sisk TM, Bühring SI, Hinrichs KU, Krumholz LR (2007) Phylogenetic and metabolic diversity of Planctomycetes from anaerobic, sulfide- and sulfur-rich Zodletone Spring, Oklahoma. Appl Environ Microbiol 73(15):4707–16

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Bryant DA, Liu Z, Li T, Zhao F, Garcia Costas AM, Klatt CG (2012) Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria. In: Burnap RL, Vermaas W (eds) Functional Genomics and Evolution of Photosynthetic Systems, vol 35. Springer, Dordrecht, pp 47–102

    Chapter  Google Scholar 

  67. Liu Z, Klatt CG, Ludwig M, Rusch DB, Jensen SI, Kühl M, Ward DM, Bryant DA (2012) “Candidatus Thermochlorobacter aerophilum:” an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics. ISME J 6(10):1869–1882

  68. Troussellier M, Schäfer H, Batailler N, Bernard L, Courties L, Lebaron P, Muyzer G, Servais P, Stackebrandt E, Vives-Rego J (2002) Bacterial activity and genetic richness along an estuarine gradient (Rhone River plume, France). Aquat Microb Ecol 28:13–24

    Article  Google Scholar 

  69. Hannig M, Braker G, Dippner J, Jürgens K (2006) Linking denitrifier community structure and prevalent biogeochemical parameters in the pelagial of the central Baltic Proper (Baltic Sea). FEMS Microbiol Ecol 57:260–271

    Article  CAS  PubMed  Google Scholar 

  70. Tiedje JM (1998) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley Sons, New Yorkpp, pp 179–244

    Google Scholar 

  71. Richardson R, Felgate H, Watmough N, Thomson A, Baggs E (2009) Mitigating release of the porent greenhouse gas N2O from the nitrogen cycle could enzymic regulation hold the key? Trends Biotechnol 27(7):388–397

    Article  CAS  PubMed  Google Scholar 

  72. Jones CM, Stres M, Rosenquist M, Hallin S (2008) Phylogenetic analysis of nitrite, nitric oxide and nitrous oxide respitory enzymes reveal a complex evolutionary history for denitrification. Mol Biol Evol 25(9):1955–1966

    Article  CAS  PubMed  Google Scholar 

  73. Kalhuzhnaya M (2013) Highly efficient methane biocatalysis revealed in a methanotrophic bacterium. Nat Commun 4:2785

    Google Scholar 

  74. Grossart HP, Frindte K, Dziallas C, Eckert W, Tang KW (2011) Microbial methane production in oxygenated water column of an oligotrophic lake. Proc Natl Acad Sci USA 108(49):19657–61

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. Tang KT, McGinnis DF, Frindte K, Brüchert V, Grossart H-P (2014) Paradox reconsidered: methane oversaturation in well-oxygenated lake waters. Limnol Oceanogr 59:275–284

    Article  Google Scholar 

  76. Sieber JR, McInerney MJ, Gunsalus RP (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66:429–52

    Article  CAS  PubMed  Google Scholar 

  77. Gray ND, Sherry A, Grant RJ, Rowan AK, Hubert CR, Callbeck CM, Aitken CM, Jones DM, Adams JJ, Larter SR, Head IM (2011) The quantitative significance of Syntrophaceae and syntrophic partnerships in methanogenic degradation of crude oil alkanes. Environ Microbiol 13(11):2957–75

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. He J, Holmes VF, Lee PKH, Alvarez-Cohen L (2007) Influence of vitamin B12 and cocultures on the growth of Dehalococcoides isolates in defined medium. Appl Environ Microbiol 73:2847–2853

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  79. Krzmarzick MJ, McNamara PJ, Crary BB, Novak PJ (2013) Abundance and diversity of organohalide-respiring bacteria in lake sediments across a geographical sulfur gradient. FEMS Microbiol Ecol 84(2):248–58

    Article  CAS  PubMed  Google Scholar 

  80. Futagami T, Okamoto F, Hashimoto H, Fukuzawa K, Higashi K, Nazir KH, Wada E, Suyama A, Takegawa K, Goto M, Nakamura K, Furukawa K (2011) Enrichment and characterization of a trichloroethene-dechlorinating consortium containing multiple "dehalococcoides" strains. Biosci Biotechnol Biochem 75(7):1268–74

    Article  CAS  PubMed  Google Scholar 

  81. Revetta RP, Matlib RS, Santo Domingo JW (2011) 16S rRNA gene sequence analysis of drinking water using RNA and DNA extracts as targets for clone library development. Curr Microbiol 63:50–59

    Article  CAS  PubMed  Google Scholar 

  82. Caporaso JG, Paszkiewicz K, Field D, Knight R, Gilbert JA (2011) The Western English Channel contains a persistent microbial seed bank. ISME J 6(6):1089–1093

    Article  PubMed Central  PubMed  Google Scholar 

  83. O’dor RK, Fennel K, VandenBerghe E (2009) A one ocean model of biodiversity. Deep-Sea Res II 56:1816–1823

    Article  Google Scholar 

  84. Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic Soda Lake in California. Appl Environ Microbiol 69:1030–1042

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  85. Székely AJ, Berga M, Langenheder S (2013) Mechanisms determining the fate of dispersed bacterial communities in new environments. ISME J 7(1):61–71

    Article  PubMed Central  PubMed  Google Scholar 

  86. Comeau AM, Harding T, Galand PE, Vincent WF, Lovejoy C (2012) Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters. Sci Rep 2:604

    Article  PubMed Central  PubMed  Google Scholar 

  87. Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49(4):359–378

    PubMed Central  CAS  PubMed  Google Scholar 

  88. Krause E, Wichels A, Gimenez L, Lunau M, Schilhabel MB, Gerdts G (2012) Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS ONE 7(10), e47035. doi:10.1371/journal.pone.0047035

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

In addition to the authors of this paper, the Lake Kivu consortium includes the following individuals: S. Bouillon (KatholiekeUniversiteit Leuven), M.-V. Commarieu, F. A. E. Roland (Université de Liège), B. Leporcq, K. de Saedeleer (Université de Namur), A. Anzil, S. Vanderschueren, C. Michiels (UniversitéLibre de Bruxelles), and G. Alunga (DR Congo team). The consortium gratefully acknowledges the Rwanda Energy Company and Michel Halbwachs for free access to their industrial platform off Gisenyi. R. Trias (Institut de Physique du Globe de Paris, France) is acknowledged for supplying some of the qPCR-positive controls. This work was funded by the Fonds National de la RechercheScientifique (FNRS) under the MICKI (Microbial diversity and processes in Lake Kivu) project and the Belgian Federal Science Policy Office EAGLES (East African Great Lake Ecosystem Sensitivity to changes, SD/AR/02A) project, and contributes the European Research Council starting grant project AFRIVAL (African river basins: Catchment-scale carbon fluxes and transformations, 240002).

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Correspondence to Özgul İnceoğlu.

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Table S1

Diversity indices for bacterial OTUs in the analyzed water column. (DOC 87 kb)

Table S2

Diversity indices for archaeal OTUs in the analyzed water column. (DOC 88 kb)

Figure S1

Rank-abundance plots based on present and active bacterial OTUs at a dissimilarity level of 3 % at depths of 10 and 100 m during September 2012. (PDF 121 kb)

Figure S2

Vertical depth profiles of different DNA- and RNA-based bacterial taxa related to different biogeochemical processes from September 2012 water samples: (a) Actinobacteria, (a) Cyanobacteria, (c) Planctomycetes, (d) Nitrospira, (e) Methylococcales, (f) Desulfobacterales and Desulfuromonadales, (g) Epsilonproteobacteria, (h) Dehalococcoidaceae (i) Chlorobi, (j) Methanomicrobia and Methanobacteria. The transition zone is indicated with a gray shade. (PDF 33 kb)

Figure S3

Hierarchical clustering of Bray-Curtis similarities of the archaeal community composition at OTU level retrieved by pyrosequencing of both DNA (black symbols) and RNA (grey symbols) nucleic acid pools in (A) February and (B) September. Samples were grouped according to oxygen content as: oxic (triangles), transition (dots), and anoxic (squares). (PDF 14 kb)

Figure S4

Network analyses of co-occurring shared bacterial (circles) and archaeal (squares) OTUs in the anoxic zone basedon correlation analyses. A connection stands for a strong (Pearson r >0.8) and significant (p-value 0.01) correlation. The size of each node is proportional to the number of connections (i.e., degree). (PDF 20 kb)

Figure S5

Relationship between occupancy (i.e., niche breadth) and relative abundance of (a) DNA-based and (b) RNA-based bacterial communitiesin the water column of Lake Kivu.High niche breadth values are indicative for habitat generalists whereas low values can be assigned to habitat specialists. (PDF 197 kb)

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İnceoğlu, Ö., Llirós, M., Crowe, S.A. et al. Vertical Distribution of Functional Potential and Active Microbial Communities in Meromictic Lake Kivu. Microb Ecol 70, 596–611 (2015). https://doi.org/10.1007/s00248-015-0612-9

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