A mesophilic, autotrophic, ammonia-oxidizing archaeon of thaumarchaeal group I.1a cultivated from a deep oligotrophic soil horizon

Applied and Environmental Microbiology

Volumn 80, Issue 12, 2014, Pages 3645-3655

  Jung, Man Young ^a   Park, Soo Je ^b   Kim, So Jeong ^a   Kim, Jong Geol ^a   Sinninghe Damsté, Jaap S ^c   Jeon, Che Ok ^d   Rhee, Sung Keun ^a  

^a Chungbuk National University   (South Korea)

^b Jeju National University   (South Korea)

^c ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^d Chung Ang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; GROUNDWATER; MICROORGANISMS; OXIDATION; RNA; SIGNAL TRANSDUCTION; SOILS;

16S RRNA GENE SEQUENCE; AMMONIA OXIDATION; AMMONIA OXIDIZERS; CARBON FIXATION; CHEMOLITHOAUTOTROPHIC; OPTIMUM TEMPERATURE; ORTHOLOGOUS GENES; TERRESTRIAL ENVIRONMENTS;

AMMONIA;

AMMONIA; ARCHAEAL DNA; NITRITE; RNA 16S; SOIL;

ARCHAEAL GENOME; ARCHAEON; CHEMISTRY; CHEMOAUTOTROPHY; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PH; PHYLOGENY; SOIL; TEMPERATURE;

AMMONIA; ARCHAEA; CHEMOAUTOTROPHIC GROWTH; DNA, ARCHAEAL; GENOME, ARCHAEAL; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; NITRITES; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SOIL; SOIL MICROBIOLOGY; TEMPERATURE;

EID: 84901335344     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03730-13     Document Type: Article

References (72)

1. Könneke M, Bernhard AE, De la Torre JR, Walker CB, Waterbury JB, Stahl DA. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543-546. http://dx.doi.org/10.1038/nature03911.
2. Chen XP, Zhu YG, Xia Y, Shen JP, He JZ. 2008. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ. Microbiol. 10:1978-1987. http://dx.doi.org/10.1111/j.1462-2920.2008.01613.x.
3. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C. 2006. Archaea predominate among ammonia- oxidizing prokaryotes in soils. Nature 442:806-809. http://dx.doi.org /10.1038/nature04983.
4. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C. 2005. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ. Microbiol. 7:1985-1995. http://dx.doi.org/10.1111/j.1462-2920 .2005.00906.x.
5. Auguet JC, Barberan A, Casamayor EO. 2010. Global ecological patterns in uncultured archaea. ISME J. 4:182-190. http://dx.doi.org/10.1038 /ismej.2009.109.
6. 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. 5:787-797. http://dx.doi.org/10.1046/j.1462-2920.2003.00476.x.
7. Verhamme DT, Prosser JI, Nicol GW. 2011. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5:1067-1071. http://dx.doi.org/10.1038 /ismej.2010.191.
8. Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI. 2010. Autotrophic ammonia oxidation by soil thaumarchaea. Proc. Natl. Acad. Sci. U. S. A. 107:17240-17245. http://dx.doi.org/10.1073/pnas .1004947107.
9. Offre P, Prosser JI, Nicol GW. 2009. Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol. Ecol. 70:99-108. http://dx.doi.org/10.1111/j.1574-6941.2009.00725.x.
10. Jung MY, Park SJ, Min D, Kim JS, Rijpstra WI, Sinninghe Damste JS, Kim GJ, Madsen EL, Rhee SK. 2011. Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Appl. Environ. Microbiol. 77:8635- 8647. http://dx.doi.org/10.1128/AEM.05787-11.
11. Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW. 2011 Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc. Natl. Acad. Sci. U. S. A. 108:15892-15897. http: //dx.doi.org/10.1073/pnas.1107196108.
12. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. U. S. A. 105:2134- 2139. http://dx.doi.org/10.1073/pnas.0708857105.
13. French E, Kozlowski JA, Mukherjee M, Bullerjahn G, Bollmann A. 2012. Ecophysiological characterization of ammonia-oxidizing archaea and bacteria from freshwater. Appl. Environ. Microbiol. 78:5773-5780. http://dx.doi.org/10.1128/AEM.00432-12.
14. Kim JG, Jung MY, Park SJ, Rijpstra WI, Sinninghe Damste JS, Madsen EL, Min D, Kim JS, Kim GJ, Rhee SK. 2012. Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environ. Microbiol. 14:1528-1543. http://dx .doi.org/10.1111/j.1462-2920.2012.02740.x.
15. Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C. 2011. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl. Acad. Sci. U. S. A. 108:8420-8425. http://dx.doi.org/10.1073 /pnas.1013488108.
16. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y-I, Sugahara J, Preston C, de la Torre J, Richardson PM, DeLong EF. 2006. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl. Acad. Sci. U. S. A. 103:18296-18301. http://dx.doi .org/10.1073/pnas.0608549103.
17. Kim BK, Jung MY, Yu DS, Park SJ, Oh TK, Rhee SK, Kim JF. 2011. Genome sequence of an ammonia-oxidizing soil archaeon, "Candidatus Nitrosoarchaeum koreensis" MY1. J. Bacteriol. 193:5539-5540. http://dx .doi.org/10.1128/JB.05717-11.
18. 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 distrib-uted marine crenarchaea. Proc. Natl. Acad. Sci. U. S. A. 107:8818-8823. http://dx.doi.org/10.1073/pnas.0913533107.
19. Mosier AC, Allen EE, Kim M, Ferriera S, Francis CA. 2012. Genome sequence of "Candidatus Nitrosoarchaeum limnia" BG20, a low-salinity ammonia-oxidizing archaeon from the San Francisco Bay estuary. J. Bacteriol. 194:2119-2120. http://dx.doi.org/10.1128/JB.00007-12.
20. Blainey PC, Mosier AC, Potanina A, Francis CA, Quake SR. 2011. Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6:e16626. http://dx.doi .org/10.1371/journal.pone.0016626.
21. Spang A, Poehlein A, Offre P, Zumbragel S, Haider S, Rychlik N, Nowka B, Schmeisser C, Lebedeva EV, Rattei T, Bohm C, Schmid M, Galushko A, Hatzenpichler R, Weinmaier T, Daniel R, Schleper C, Spieck E, Streit W, Wagner M. 2012. The genome of the ammoniaoxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ. Microbiol. 14:3122- 3145. http://dx.doi.org/10.1111/j.1462-2920.2012.02893.x.
22. Bartossek R, Nicol GW, Lanzen A, Klenk HP, Schleper C. 2010. Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context. Environ. Microbiol. 12:1075-1088. http://dx.doi .org/10.1111/j.1462-2920.2010.02153.x.
23. Bartossek R, Spang A, Weidler G, Lanzen A, Schleper C. 2012. Metagenomic analysis of ammonia-oxidizing archaea affiliated with the soil group. Front. Microbiol. 3:208. http://dx.doi.org/10.3389/fmicb.2012 .00208.
24. Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S, He JZ. 2010. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol. Ecol. 72:386-394. http://dx.doi.org/10.1111/j.1574-6941.2010.00861.x.
25. Jia Z, Conrad R. 2009. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11:1658- 1671. http://dx.doi.org/10.1111/j.1462-2920.2009.01891.x.
26. Brady NC, Weil RR. 2007. The nature and properties of soils, 14th ed. Pearson Prentice Hall, Upper Saddle River, NJ.
27. Jung MY, Well R, Min D, Giesemann A, Park SJ, Kim JG, Kim SJ, Rhee SK. 14 November 2013. Isotopic signatures of N2O produced by ammonia- oxidizing archaea from soils. ISME J. http://dx.doi.org/10.1038/ismej .2013.205.
28. Shinn MB. 1941. Colorimetric method for determination of nitrate. Ind. Chem. Anal. Engl. Ed. 13:33-35. http://dx.doi.org/10.1021/i560089a010.
29. Hynes RK, Knowles R. 1984. Production of nitrous oxide by Nitrosomonas europaea: effects of acetylene, pH, and oxygen. Can. J. Microbiol. 30:1397-1404. http://dx.doi.org/10.1139/m84-222.
30. Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S, He JZ. 2009. Nitrification driven by Bacteria and not Archaea in nitrogen- rich grassland soils. Nat. Geosci. 2:621-624. http://dx.doi.org/10 .1038/ngeo613.
31. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188-7196. http://dx.doi.org/10.1093/nar/gkm864.
32. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882. http://dx.doi.org/10.1093/nar/25.24.4876.
33. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
34. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120. http://dx.doi.org/10.1007/BF01731581.
35. Pitcher A, Rychlik N, Hopmans EC, Spieck E, Rijpstra WI, Ossebaar J, Schouten S, Wagner M, Damste JS. 2010. Crenarchaeol dominates the membrane lipids of Candidatus Nitrososphaera gargensis, a thermophilic group I.1b archaeon. ISME J. 4:542-552. http://dx.doi.org/10.1038/ismej .2009.138.
36. Schouten S, Huguet C, Hopmans EC, Kienhuis MV, Sinninghe Damsté JS. 2007. Analytical methodology for TEX86 paleothermometry by highperformance liquid chromatography/atmospheric pressure chemical ionization- mass spectrometry. Anal. Chem. 79:2940-2944. http://dx.doi.org /10.1021/ac062339v.
37. 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. 65:5554-5563.
38. Alm EW, Oerther DB, Larsen N, Stahl DA, Raskin L. 1996. The oligonucleotide probe database. Appl. Environ. Microbiol. 62:3557-3559.
39. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919-1925.
40. Reynolds ES. 1963. The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J. Cell Biol. 17:208-212. http://dx .doi.org/10.1083/jcb.17.1.208.
41. Zhou J, Bruns MA, Tiedje JM. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62:316-322.
42. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
43. Yu C, Zavaljevski N, Desai V, Reifman J. 2009. Genome-wide enzyme annotation with precision control: catalytic families (CatFam) databases. Proteins 74:449-460. http://dx.doi.org/10.1002/prot.22167.
44. Tatusov RL, Galperin MY, Natale DA, Koonin EV. 2000. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28:33-36. http://dx.doi.org/10.1093/nar/28.1.33.
45. Pruitt KD, Tatusova T, Maglott DR. 2007. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35:D61-D65. http://dx.doi.org/10 .1093/nar/gkl842.
46. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch GD, Rodionov DA, Ruckert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y, Zagnitko O, Vonstein V. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33:5691-5702. http://dx.doi.org/10.1093/nar /gki866.
47. Konstantinidis KT, Tiedje JM. 2005. Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. U. S. A. 102:2567- 2572. http://dx.doi.org/10.1073/pnas.0409727102.
48. von Wintzingerode F, Gobel UB, Stackebrandt E. 1997. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol. Rev. 21:213-229. http://dx.doi.org/10 .1111/j.1574-6976.1997.tb00351.x.
49. Gundersen K. 1955. Effects of B-vitamins and ammo-acids on nitrification. Physiol. Plant. 8:136-141. http://dx.doi.org/10.1111/j.1399-3054 .1955.tb08966.x.
50. Jones RD, Hood M. 1980. Effects of temperature, pH, salinity, and inorganic nitrogen on the rate of ammonium oxidation by nitrifiers isolated from wetland environments. Microb. Ecol. 6:339-347. http://dx.doi.org /10.1007/BF02010496.
51. Cole JJ. 1982. Interactions between Bacteria and Algae in aquatic ecosystems. Annu. Rev. Ecol. Syst. 13:291-314. http://dx.doi.org/10.1146 /annurev.es.13.110182.001451.
52. Hube AE, Heyduck-Söller B, Fischer U. 2009. Phylogenetic classification of heterotrophic bacteria associated with filamentous marine cyanobacteria in culture. Syst. Appl. Microbiol. 32:256-265. http://dx.doi.org/10 .1016/j.syapm.2009.03.001.
53. Pitcher A, Hopmans EC, Mosier AC, Park SJ, Rhee SK, Francis CA, Schouten S, Damste JS. 2011. Core and intact polar glycerol dibiphytanyl glycerol tetraether lipids of ammonia-oxidizing archaea enriched from marine and estuarine sediments. Appl. Environ. Microbiol. 77:3468- 3477. http://dx.doi.org/10.1128/AEM.02758-10.
54. Sinninghe Damsté JS, Rijpstra WIC, Hopmans EC, Jung M-Y, Kim J-G, Rhee S-K, Stieglmeier M, Schleper C. 2012. Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids of group I.1a and I.1b thaumarchaeota in soil. Appl. Environ. Microbiol. 78:6866-6874. http://dx.doi .org/10.1128/AEM.01681-12.
55. Lehtovirta-Morley LE, Verhamme DT, Nicol GW, Prosser JI. 2013. Effect of nitrification inhibitors on the growth and activity of Nitrosotalea devanaterra in culture and soil. Soil Biol. Biochem. 62:129-133. http://dx .doi.org/10.1016/j.soilbio.2013.01.020.
56. Shen T, Stieglmeier M, Dai J, Urich T, Schleper C. 2013. Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiol. Lett. 344:121-129. http://dx.doi .org/10.1111/1574-6968.12164.
57. Stock AM, Robinson VL, Goudreau PN. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183-215. http://dx.doi.org/10 .1146/annurev.biochem.69.1.183.
58. Schleper C, Jurgens G, Jonuscheit M. 2005. Genomic studies of uncultivated archaea. Nat. Rev. Microbiol. 3:479-488. http://dx.doi.org/10 .1038/nrmicro1159.
59. Park SJ, Kim JG, Jung MY, Kim SJ, Cha IT, Ghai R, Martin-Cuadrado AB, Rodriguez-Valera F, Rhee SK. 2012. Draft genome sequence of an ammonia-oxidizing archaeon, "Candidatus Nitrosopumilus sediminis" AR2, from Svalbard in the Arctic Circle. J. Bacteriol. 194:6948-6949. http: //dx.doi.org/10.1128/JB.01869-12.
60. Vajrala N, Martens-Habbena W, Sayavedra-Soto LA, Schauer A, Bottomley PJ, Stahl DA, Arp DJ. 2013. Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. Proc. Natl. Acad. Sci. U. S. A. 110:1006-1011. http://dx.doi.org/10.1073/pnas .1214272110.
61. Amano F, Noda T. 1995. Improved detection of nitric oxide radical (NO) production in an activated macrophage culture with a radical scavenger, carboxy PTIO and Griess reagent. FEBS Lett. 368:425-428. http://dx.doi .org/10.1016/0014-5793(95)00700-J.
62. Ellis A, Lu H, Li CG, Rand MJ. 2001. Effects of agents that inactivate free radical NO (NO) on nitroxyl anion-mediated relaxations, and on the detection of NO released from the nitroxyl anion donor Angeli's salt. Br. J. Clin. Pharmacol. 134:521-528. http://dx.doi.org/10.1038/sj.bjp .0704287.
63. Samuni U, Samuni Y, Goldstein S. 2010. On the distinction between nitroxyl and nitric oxide using nitronyl nitroxides. J. Am. Chem. Soc. 132:8428-8432. http://dx.doi.org/10.1021/ja101945j.
64. Berg IA, Kockelkorn D, Buckel W, Fuchs G. 2007. A 3-hydroxypropionate/ 4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318:1782-1786. http://dx.doi.org/10.1126 /science.1149976.
65. Mosier AC, Lund MB, Francis CA. 2012. Ecophysiology of an ammoniaoxidizing archaeon adapted to low-salinity habitats. Microb. Ecol. 64:955- 963. http://dx.doi.org/10.1007/s00248-012-0075-1.
66. Amin US, Lash TD, Wilkinson BJ. 1995. Proline betaine is a highly effective osmoprotectant for Staphylococcus aureus. Arch. Microbiol. 163:138-142. http://dx.doi.org/10.1007/BF00381788.
67. Roth WG, Leckie MP, Dietzler DN. 1985. Osmotic stress drastically inhibits active transport of carbohydrates by Escherichia coli. Biochem. Biophys. Res. Commun. 126:434-441. http://dx.doi.org/10.1016/0006 -291X(85)90624-2.
68. Martin DD, Ciulla RA, Roberts MF. 1999. Osmoadaptation in Archaea. Appl. Environ. Microbiol. 65:1815-1825.
69. Park SJ, Kim JG, Jung MY, Kim SJ, Cha IT, Kwon K, Lee JH, Rhee SK. 2012. Draft genome sequence of an ammonia-oxidizing archaeon, "Candidatus Nitrosopumilus koreensis" AR1, from marine sediment. J. Bacteriol. 194:6940-6941. http://dx.doi.org/10.1128/JB.01857-12.
70. Tourna M, Freitag TE, Nicol GW, Prosser JI. 2008. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ. Microbiol. 10:1357-1364. http://dx.doi.org/10 .1111/j.1462-2920.2007.01563.x.
71. Daebeler A, Abell GC, Bodelier PL, Bodrossy L, Frampton DM, Hefting MM, Laanbroek HJ. 2012. Archaeal dominated ammonia-oxidizing communities in Icelandic grassland soils are moderately affected by longtermNfertilization and geothermal heating. Front. Microbiol. 3:352. http: //dx.doi.org/10.3389/fmicb.2012.00352.
72. Lebedeva EV, Hatzenpichler R, Pelletier E, Schuster N, Hauzmayer S, Bulaev A, Grigor'eva NV, Galushko A, Schmid M, Palatinszky M, Le Paslier D, Daims H, Wagner M. 2013. Enrichment and genome sequence of the group I.1a ammonia-oxidizing archaeon "Ca. Nitrosotenuis uzonensis" representing a clade globally distributed in thermal habitats. PLoS One 8:e80835. http://dx.doi.org/10.1371/journal.pone.0080835.