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Why Archaea Are Limited in Their Exploitation of Other, Living Organisms

  • Stephen T. Abedon
Chapter

Abstract

Only a handful of Archaea have been suggested to be connected with pathologies or to serve as parasites, and none conclusively. Here I consider what might limit the potential for Archaea to serve as exploiters of other, living organisms. I suggest that this dearth may be a consequence of multiple factors which have a combined impact rather than any one factor serving as a ‘smoking gun’. These factors should be viewed as hypotheses, further exploration of which may be helpful towards refinement of considerations of just what may serve to limit the occurrence of Archaea serving as pathogens. I suggest as well that a spectrum likely exists in which eukaryotes—among the three cellular domains—are most frequently exploitive of other species while Archaea are the least. Bacteria, when serving especially as pathogens but also as predators, in turn display an intermediate propensity to exploit other organisms.

Keywords

Horizontal gene exchange Infectious dose Mutation rates Niche invasion Oligotrophy Organotrophy Population sizes 

Notes

Acknowledgements

I am grateful to John Reeve for both introducing me to the issue of rarity of pathogens among Archaea and also for helpful discussion of the ideas presented in this and a previously published essay on this subject.

References

  1. Abedon ST (2013) Are archaeons incapable of being parasites or have we simply failed to notice? Bioessays: news and reviews in molecular. Cell Dev Biol 35:501Google Scholar
  2. Aller JY, Kemp PF (2008) Are archaea inherently less diverse than bacteria in the same environments? FEMS Microbiol Ecol 65:74–87CrossRefPubMedGoogle Scholar
  3. Aminov RI (2013) Role of archaea in human disease. Front Cell Infect Microbiol 3:42CrossRefPubMedPubMedCentralGoogle Scholar
  4. Andrei AS, Banciu HL, Oren A (2012) Living with salt: metabolic and phylogenetic diversity of archaea inhabiting saline ecosystems. FEMS Microbiol Lett 330:1–9CrossRefPubMedGoogle Scholar
  5. Andrei AS, Robeson MS, Baricz A, Coman C, Muntean V, Ionescu A, Etiope G, Alexe M, Sicora CI, Podar M, Banciu HL (2015) Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes. ISME J 9:2642–2656CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bang C, Schmitz RA (2015) Archaea associated with human surfaces: not to be underestimated. FEMS Microbiol Rev 39:631–648CrossRefPubMedGoogle Scholar
  7. Barash I, Manulis-Sasson S (2009) Recent evolution of bacterial pathogens: the gall-forming Pantoea agglomerans case. Annu Rev Phytopathol 47:133–152CrossRefPubMedGoogle Scholar
  8. Baricz A, Coman C, Andrei AS, Muntean V, Keresztes ZG, Pausan M, Alexe M, Banciu HL (2014) Spatial and temporal distribution of archaeal diversity in meromictic, hypersaline Ocnei Lake (Transylvanian Basin, Romania). Extremophiles 18:399–413CrossRefPubMedGoogle Scholar
  9. Bates ST, Berg-Lyons D, Caporaso JG, Waters WA, Knight R, Fierer N (2011) Examining the global distrbiution of dominant archaeal populations in soil. ISME J 5:908–917CrossRefPubMedGoogle Scholar
  10. Bokhari H, Anwar M, Mirza HB, Gillevet PM (2011) Evidences of lateral gene transfer between archaea and pathogenic bacteria. Bioinformation 6:293–296CrossRefPubMedPubMedCentralGoogle Scholar
  11. Borrel G, Lehours AC, Crouzet O, Jezequel D, Rockne K, Kulczak A, Duffaud E, Joblin K, Fonty G (2012) Stratification of Archaea in the deep sediments of a freshwater meromictic lake: vertical shift from methanogenic to uncultured archaeal lineages. PLoS ONE 7:e43346CrossRefPubMedPubMedCentralGoogle Scholar
  12. Brown SP, Inglis RF (2009) Evolutionary ecology of microbial wars: within-host competition and (incidental) virulence. Evol Appl 2:32–39CrossRefPubMedPubMedCentralGoogle Scholar
  13. Buée M, De Boer W, Martin F, van Overbeek L, Jurkevitch E (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212CrossRefGoogle Scholar
  14. Calcagno V, Dubosclard M, de MC (2010) Rapid exploiter-victim coevolution: the race is not always to the swift. Am Nat 176:198–211Google Scholar
  15. Cao P, Zhang LM, Shen JP, Zheng YM, Di HJ, He JZ (2012) Distribution and diversity of archaeal communities in selected Chinese soils. FEMS Microbiol Ecol 80:146–158CrossRefPubMedGoogle Scholar
  16. Casadevall A, Pirofski LA (2000) Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection, and disease. Infect Immun 68:6511–6518CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cavicchioli R, Curmi PM (2004) Response to William Martin’s letter. Bioessays 26:593Google Scholar
  18. Cavicchioli R, Curmi PM, Saunders N, Thomas T (2003) Pathogenic archaea: do they exist? Bioessays (News and Reviews In Molecular Cellular and Developmental Biology) 25:1119–1128CrossRefGoogle Scholar
  19. Chaban B, Ng SY, Jarrell KF (2006) Archaeal habitats—from the extreme to the ordinary. Can J Microbiol 52:73–116CrossRefPubMedGoogle Scholar
  20. Chen L, Brugger K, Skovgaard M, Redder P, She Q, Torarinsson E, Greve B, Awayez M, Zibat A, Klenk HP, Garrett RA (2005) The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J Bacteriol 187:4992–4999CrossRefPubMedPubMedCentralGoogle Scholar
  21. Choi IG, Kim SH (2007) Global extent of horizontal gene transfer. Proc Natl Acad Sci U S A 104:4489–4494CrossRefPubMedPubMedCentralGoogle Scholar
  22. Christie GE, Allison HA, Kuzio J, McShan M, Waldor MK, Kropinski AM (2012) Prophage-induced changes in cellular cytochemistry and virulence. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 33–60CrossRefGoogle Scholar
  23. Conway de Macario E, Macario AJL (2009) Methanogenic archaea in health and disease: a novel paradigm of microbial pathogenesis. Int J Med Microbiol 299:99–108CrossRefPubMedGoogle Scholar
  24. Curtis TP, Sloan WT (2004) Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr Opin Microbiol 7:221–226CrossRefPubMedGoogle Scholar
  25. DeLong EF, Taylor LT, Marsh TL, Preston CM (1999) Visualization and enumeration of marine planktonic archaea and bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl Environ Microbiol 65:5554–5563PubMedPubMedCentralGoogle Scholar
  26. Eckburg PB, Lepp PW, Relman DA (2003) Archaea and their potential role in human disease. Infect Immun 71:591–596CrossRefPubMedPubMedCentralGoogle Scholar
  27. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science (New York, N Y) 308:1635–1638Google Scholar
  28. Ewald PW (2004) Evolution of virulence. Infect Dis Clin North Am 18:1–15CrossRefPubMedGoogle Scholar
  29. Faguy DM (2003) Lateral gene transfer (LGT) between Archaea and Escherichia coli is a contributor to the emergence of novel infectious disease. BMC Infect Dis 3:13CrossRefPubMedPubMedCentralGoogle Scholar
  30. Fellous S, Salvaudon L (2009) How can your parasites become your allies? Trends Parasitol 25:62–66CrossRefPubMedGoogle Scholar
  31. Fredriksson NJ, Hermansson M, Wilen BM (2012) Diversity and dynamics of archaea in an activated sludge wastewater treatment plant. BMC Microbiol 12:140CrossRefPubMedPubMedCentralGoogle Scholar
  32. Fredriksson NJ, Hermansson M, Wilen BM (2013) The choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PLoS ONE 8:e76431CrossRefPubMedPubMedCentralGoogle Scholar
  33. Giannone RJ, Wurch LL, Heimerl T, Martin S, Yang Z, Huber H, Rachel R, Hettich RL, Podar M (2015) Life on the edge: functional genomic response of Ignicoccus hospitalis to the presence of Nanoarchaeum equitans. ISME J 9:101–114Google Scholar
  34. Gill EE, Brinkman FS (2011) The proportional lack of archaeal pathogens: Do viruses/phages hold the key? Bioessays 33:248–254Google Scholar
  35. Golyshina OV, Lunsdorf H, Kublanov IV, Goldenstein NI, Hinrichs KU, Golyshin PN (2016) The novel extremely acidophilic, cell-wall-deficient archaeon Cuniculiplasma divulgatum gen. nov., sp. nov. represents a new family, Cuniculiplasmataceae fam. nov., of the order Thermoplasmatales. Int J Syst Evol Microbiol 66:332–340CrossRefPubMedPubMedCentralGoogle Scholar
  36. Gophna U, Charlebois RL, Doolittle WF (2004) Have archaeal genes contributed to bacterial virulence? Trends Microbiol 12:213–219CrossRefPubMedGoogle Scholar
  37. Groisman EA, Ochman H (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87:791–794CrossRefPubMedGoogle Scholar
  38. Groussin M, Boussau B, Szollosi G, Eme L, Gouy M, Brochier-Armanet C, Daubin V (2016) Gene acquisitions from bacteria at the origins of major archaeal clades are vastly overestimated. Mol Biol Evol 33:305–310CrossRefPubMedGoogle Scholar
  39. Hagman M, Nielsen JL, Nielsen PH, Jansen J (2008) Mixed carbon sources for nitrate reduction in activated sludge-identification of bacteria and process activity studies. Water Res 42:1539–1546CrossRefPubMedGoogle Scholar
  40. Herndl GJ, Reinthaler T, Teira E, van AH, Veth C, Pernthaler A, Pernthaler J (2005) Contribution of archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 71:2303–2309Google Scholar
  41. Holder T, Basquin C, Ebert J, Randel N, Jollivet D, Conti E, Jekely G, Bono F (2013) Deep transcriptome-sequencing and proteome analysis of the hydrothermal vent annelid Alvinella pompejana identifies the CvP-bias as a robust measure of eukaryotic thermostability. Biol Direct 8:2CrossRefPubMedPubMedCentralGoogle Scholar
  42. Horz HP, Conrads G (2010) The discussion goes on: what is the role of Euryarchaeota in humans? Archaea 2010:967271CrossRefPubMedPubMedCentralGoogle Scholar
  43. Jahn U, Gallenberger M, Paper W, Junglas B, Eisenreich W, Stetter KO, Rachel R, Huber H (2008) Nanoarchaeum equitans and Ignicoccus hospitalis: new insights into a unique, intimate association of two archaea. J Bacteriol 190:1743–1750CrossRefPubMedGoogle Scholar
  44. Karlsson AE, Johansson T, Bengtson P (2012) Archaeal abundance in relation to root and fungal exudation rates. FEMS Microbiol Ecol 80:305–311CrossRefPubMedGoogle Scholar
  45. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature (London) 409:507–510CrossRefGoogle Scholar
  46. Klappenbach JA, Saxman PR, Cole JR, Schmidt TM (2001) rrndb: the ribosomal RNA operon copy number database. Nucl Acids Res 29:181–184CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lane N, Martin W (2010) The energetics of genome complexity. Nature (London) 467:929–934CrossRefGoogle Scholar
  48. Lange M, Westermann P, Ahring BK (2005) Archaea in protozoa and metazoa. Appl Microbiol Biotechnol 66:465–474CrossRefPubMedGoogle Scholar
  49. Lawrence JG, Hendrickson H (2008) Genomes in motion: gene transfer as a catalyst for genome change. Horizontal gene transfer in the evolution of pathogenesis. Cambridge University Press, Cambridge, pp 3–22CrossRefGoogle Scholar
  50. LeClerc JE, Li B, Payne WL, Cebula TA (1996) High mutation frequencies among Escherichia coli and Salmonella pathogens. Science (New York, N Y) 274:1208–1211Google Scholar
  51. Lee ZM, Bussema C III, Schmidt TM (2009) rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucl Acids Res 37:D489–D493CrossRefPubMedGoogle Scholar
  52. Leggett HC, Cornwallis CK, West SA (2012) Mechanisms of pathogenesis, infective dose and virulence in human parasites. PLoS Pathog 8:e1002512CrossRefPubMedPubMedCentralGoogle Scholar
  53. Levin LA (2010) Anaerobic metazoans: no longer an oxymoron. BMC Biol 8:31CrossRefPubMedPubMedCentralGoogle Scholar
  54. Li WKW, Dickie PM, Irwin BD, Wood AM (1992) Biomass of bacteria, cyanobacteria, prochlorophytes and photosynthetic eukaryotes in the Sargasso Sea. Deep Sea Res Part A (Oceanographic Research Papers) 39:501–519CrossRefGoogle Scholar
  55. Li J, Zhou H, Fang J, Sun Y, Dasgupta S (2014) Microbial distribution in different spatial positions within the walls of a black sulfide hydrothermal chimney. Mar Ecol Prog Ser 508:67–85CrossRefGoogle Scholar
  56. Li D, Wang P, Wang P, Hu X, Chen F (2016) The gut microbiota: a treasure for human health. Biotechnol Adv 34:1210–1224CrossRefPubMedGoogle Scholar
  57. Lipp JS, Morono Y, Inagaki F, Hinrichs KU (2008) Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature (London) 454:991–994CrossRefGoogle Scholar
  58. Liu LJ, You XY, Guo X, Liu SJ, Jiang CY (2011) Metallosphaera cuprina sp. nov., an acidothermophilic, metal-mobilizing archaeon. Int J Syst Evol Microbiol 61:2395–2400CrossRefPubMedGoogle Scholar
  59. López-García P, Zivanovic Y, Deschamps P, Moreira D (2015) Bacterial gene import and mesophilic adaptation in archaea. Nat Rev Microbiol 13:447–456CrossRefPubMedPubMedCentralGoogle Scholar
  60. Lurie-Weinberger MN, Gophna U (2015) Archaea in and on the human body: health implications and future directions. PLoS Pathog 11:e1004833CrossRefPubMedPubMedCentralGoogle Scholar
  61. Lurie-Weinberger MN, Peeri M, Gophna U (2012a) Contribution of lateral gene transfer to the gene repertoire of a gut-adapted methanogen. Genomics 99:52–58CrossRefPubMedGoogle Scholar
  62. Lurie-Weinberger MN, Peeri M, Tuller T, Gophna U (2012b) Extensive inter-domain lateral gene transfer in the evolution of the human commensal methanosphaera stadtmanae. Front Genet 3:182CrossRefPubMedPubMedCentralGoogle Scholar
  63. Lynch M (2010) Evolution of the mutation rate. Trends Genet 26:345–352CrossRefPubMedPubMedCentralGoogle Scholar
  64. Martin W (2004) Pathogenic archaebacteria: do they not exist because archaebacteria use different vitamins? Bioessays 26:592–593Google Scholar
  65. Miller-Coleman RL, Dodsworth JA, Ross CA, Shock EL, Williams AJ, Hartnett HE, McDonald AI, Havig JR, Hedlund BP (2012) Korarchaeota diversity, biogeography, and abundance in Yellowstone and Great Basin hot springs and ecological niche modeling based on machine learning. PLoS ONE 7:e35964CrossRefPubMedPubMedCentralGoogle Scholar
  66. Moissl-Eichinger C, Huber H (2011) Archaeal symbionts and parasites. Curr Opin Mirobiol 14:364–370CrossRefGoogle Scholar
  67. Moxon R, Tang C (2000) Challenge of investigating biologically relevant functions of virulence factors in bacterial pathogens. Philos Trans R Soc Lond B Biol Sci 355:643–656CrossRefPubMedPubMedCentralGoogle Scholar
  68. Muller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, van der Giezen M, Tielens AG, Martin WF (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495CrossRefPubMedPubMedCentralGoogle Scholar
  69. Murray AE, Preston CM, Massana R, Taylor LT, Blakis A, Wu K, DeLong EF (1998) Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol 64:2585–2595PubMedPubMedCentralGoogle Scholar
  70. Nguyen-Hieu T, Khelaifia S, Aboudharam G, Drancourt M (2013) Methanogenic archaea in subgingival sites: a review. APMIS 121:467–477CrossRefPubMedGoogle Scholar
  71. Nkamga VD, Henrissat B, Drancourt M (2016) Archaea: essential inhabitants of the human digestive microbiota. Hum Microbiome J 3:1–8CrossRefGoogle Scholar
  72. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature (London) 405:299–304CrossRefGoogle Scholar
  73. Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5:787–797CrossRefPubMedGoogle Scholar
  74. Pal C, Macia MD, Oliver A, Schachar I, Buckling A (2007) Coevolution with viruses drives the evolution of bacterial mutation rates. Nature (London) 450:1079–1081CrossRefGoogle Scholar
  75. Pallen MJ, Wren BW (2007) Bacterial pathogenomics. Nature (London) 449:835–842CrossRefGoogle Scholar
  76. Pape T, Hoffmann F, Quéric N-V, von Juterzenka K, Reitner J, Michaelis W (2006) Dense populations of Archaea associated with demosponge Tentorium semisuberites Schmidt, 1870 from Arctic deep-waters. Polar Biol 29:662–667CrossRefGoogle Scholar
  77. Park JS, Simpson AG, Lee WJ, Cho BC (2007) Ultrastructure and phylogenetic placement within Heterolobosea of the previously unclassified, extremely halophilic heterotrophic flagellate Pleurostomum flabellatum (Ruinen 1938). Protist 158:397–413CrossRefPubMedGoogle Scholar
  78. Park JS, De Jonckheere JF, Simpson AG (2012) Characterization of Selenaion koniopes n. gen., n. sp., an amoeba that represents a new major lineage within heterolobosea, isolated from the Wieliczka salt mine. J Eukaryot Microbiol 59:601–613CrossRefPubMedGoogle Scholar
  79. Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR, Quail M, Smith F, Walker D, Libberton B, Fenton A, Hall N, Brockhurst MA (2010) Antagonistic coevolution accelerates molecular evolution. Nature (London) 464:275–278CrossRefGoogle Scholar
  80. Perevalova AA, Kublanov IV, Bidzhieva SK, Mukhopadhyay B, Bonch-Osmolovskaya EA, Lebedinsky AV (2016) Reclassification of Desulfurococcus mobilis as a synonym of Desulfurococcus mucosus, Desulfurococcus fermentans and Desulfurococcus kamchatkensis as synonyms of Desulfurococcus amylolyticus, and emendation of the D. mucosus and D. amylolyticus species descriptions. Int J Syst Evol Microbiol 66:514–517CrossRefPubMedGoogle Scholar
  81. Podar M, Anderson I, Makarova KS, Elkins JG, Ivanova N, Wall MA, Lykidis A, Mavromatis K, Sun H, Hudson ME, Chen W, Deciu C, Hutchison D, Eads JR, Anderson A, Fernandes F, Szeto E, Lapidus A, Kyrpides NC, Saier MH Jr, Richardson PM, Rachel R, Huber H, Eisen JA, Koonin EV, Keller M, Stetter KO (2008) A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans. Genome Biol 9:R158CrossRefPubMedPubMedCentralGoogle Scholar
  82. Podar M, Makarova KS, Graham DE, Wolf YI, Koonin EV, Reysenbach AL (2013) Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park. Biol Direct 8:9CrossRefPubMedPubMedCentralGoogle Scholar
  83. Prieur D (2002) Hydrothermal vents: prokaryotes in deep-sea hydrothermal vents. Encycl Environ Microbiol 1617–1628Google Scholar
  84. Raskin DM, Seshadri R, Pukatzki SU, Mekalanos JJ (2006) Bacterial genomics and pathogen evolution. Cell 124:703–714CrossRefPubMedGoogle Scholar
  85. Reeve JN (1999) Archaebacteria then … Archaes now (are there really no archaeal pathogens?). J Bacteriol 181:3613–3617PubMedPubMedCentralGoogle Scholar
  86. Reitschuler C, Lins P, Wagner AO, Illmer P (2014) Cultivation of moonmilk-born non-extremophilic Thaum and Euryarchaeota in mixed culture. Anaerobe 29:73–79CrossRefPubMedGoogle Scholar
  87. Rivera-Perez JI, Gonzalez AA, Toranzos GA (2017) From evolutionary advantage to disease agents: forensic reevaluation of host-microbe interactions and pathogenicity. Microbiol Spectr 5:EMF-0009-2016Google Scholar
  88. Rohmer L, Hocquet D, Miller SI (2011) Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol 19:341–348CrossRefPubMedPubMedCentralGoogle Scholar
  89. Saengkerdsub S, Ricke SC (2013) Ecology and characteristics of methanogenic archaea in animals and humans. Crit Rev MicrobiolGoogle Scholar
  90. Sahm K, John P, Nacke H, Wemheuer B, Grote R, Daniel R, Antranikian G (2013) High abundance of heterotrophic prokaryotes in hydrothermal springs of the Azores as revealed by a network of 16S rRNA gene-based methods. Extremophiles 17:649–662CrossRefPubMedGoogle Scholar
  91. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molfsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  92. Seger J (1992) Evolution of exploiter–victim relationships. In: Crawley MJ (ed) Natural enemies. The population biology of predators, parasites and diseases. Blackwell Scientific, Oxford, pp 3–25Google Scholar
  93. Selig M, Schönheit P (1994) Oxidation of organic compounds to CO2 with sulfur or thiosulfate as electron acceptor in the anaerobic hyperthermophilic archaea Thermoproteus tenax and Pyrobaculum islandicum proceeds via the citric acid cycle. Arch Microbiol 162:286–294CrossRefGoogle Scholar
  94. Shiffman ME, Charalambous BM (2012) The search for archaeal pathogens. Rev Med Microbiol 23:45–51Google Scholar
  95. Sinclair JL, Ghiorse WC (1987) Distribution of protozoa in subsurface sediments of a pristine groundwater study site in Oklahoma. Appl Environ Microbiol 53:1157–1163PubMedPubMedCentralGoogle Scholar
  96. Smets BF, Lardon L (2009) Mass action models describing extant horizontal transfer of plasmids: inferences and parameter sensitivities. Meth Mol Biol 532:289–305CrossRefGoogle Scholar
  97. Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160CrossRefPubMedPubMedCentralGoogle Scholar
  98. Tanaka T, Kawasaki K, Daimon S, Kitagawa W, Yamamoto K, Tamaki H, Tanaka M, Nakatsu CH, Kamagata Y (2014) A hidden pitfall in the preparation of agar media undermines microorganism cultivability. Appl Environ Microbiol 80:7659–7666CrossRefPubMedPubMedCentralGoogle Scholar
  99. Turkarslan S, Reiss DJ, Gibbins G, Su WL, Pan M, Bare JC, Plaisier CL, Baliga NS (2011) Niche adaptation by expansion and reprogramming of general transcription factors. Mol Syst Biol 7:554CrossRefPubMedPubMedCentralGoogle Scholar
  100. Uroz S, Oger P, Tisserand E, Cebron A, Turpault MP, Buee M, De BW, Leveau JH, Frey-Klett P (2016) Specific impacts of beech and Norway spruce on the structure and diversity of the rhizosphere and soil microbial communities. Sci Rep 6:27756CrossRefPubMedPubMedCentralGoogle Scholar
  101. Urschel MR, Kubo MD, Hoehler TM, Peters JW, Boyd ES (2015) Carbon source preference in chemosynthetic hot spring communities. Appl Environ Microbiol 81:3834–3847CrossRefPubMedPubMedCentralGoogle Scholar
  102. Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5:316–323CrossRefPubMedGoogle Scholar
  103. Wassenaar TM, Gaastra W (2001) Bacterial virulence: can we draw the line? FEMS Microbiol Lett 201:1–7CrossRefPubMedGoogle Scholar
  104. Welte C, Deppenmeier U (2011) Proton translocation in methanogens. Methods Enzymol 494:257–280CrossRefPubMedGoogle Scholar
  105. Wrede C, Dreier A, Kokoschka S, Hoppert M (2012) Archaea in symbioses. Archaea 2012:596846CrossRefPubMedPubMedCentralGoogle Scholar
  106. Xue Y, Fan H, Ventosa A, Grant WD, Jones BE, Cowan DA, Ma Y (2005) Halalkalicoccus tibetensis gen. nov., sp. nov., representing a novel genus of haloalkaliphilic archaea. Int J Syst Evol Microbiol 55:2501–2505CrossRefPubMedGoogle Scholar
  107. Yau S, Lauro FM, Williams TJ, Demaere MZ, Brown MV, Rich J, Gibson JA, Cavicchioli R (2013) Metagenomic insights into strategies of carbon conservation and unusual sulfur biogeochemistry in a hypersaline Antarctic lake. ISME J 7:1944–1961CrossRefPubMedPubMedCentralGoogle Scholar
  108. Ziebuhr W, Hennig S, Eckart M, Kranzler H, Batzilla C, Kozitskaya S (2006) Nosocomial infections by Staphylococcus epidermidis: how a commensal bacterium turns into a pathogen. Int J Antimicrob Agents 28(Suppl 1):S14–S20CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of MicrobiologyThe Ohio State UniversityMansfieldUSA

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