Microbial Ecology

, Volume 77, Issue 3, pp 559–573 | Cite as

Bacterial Diversity in Replicated Hydrogen Sulfide-Rich Streams

  • Scott Hotaling
  • Corey R. Quackenbush
  • Julian Bennett-Ponsford
  • Daniel D. New
  • Lenin Arias-Rodriguez
  • Michael Tobler
  • Joanna L. KelleyEmail author
Microbiology of Aquatic Systems


Extreme environments typically require costly adaptations for survival, an attribute that often translates to an elevated influence of habitat conditions on biotic communities. Microbes, primarily bacteria, are successful colonizers of extreme environments worldwide, yet in many instances, the interplay between harsh conditions, dispersal, and microbial biogeography remains unclear. This lack of clarity is particularly true for habitats where extreme temperature is not the overarching stressor, highlighting a need for studies that focus on the role other primary stressors (e.g., toxicants) play in shaping biogeographic patterns. In this study, we leveraged a naturally paired stream system in southern Mexico to explore how elevated hydrogen sulfide (H2S) influences microbial diversity. We sequenced a portion of the 16S rRNA gene using bacterial primers for water sampled from three geographically proximate pairings of streams with high (> 20 μM) or low (~ 0 μM) H2S concentrations. After exploring bacterial diversity within and among sites, we compared our results to a previous study of macroinvertebrates and fish for the same sites. By spanning multiple organismal groups, we were able to illuminate how H2S may differentially affect biodiversity. The presence of elevated H2S had no effect on overall bacterial diversity (p = 0.21), a large effect on community composition (25.8% of variation explained, p < 0.0001), and variable influence depending upon the group—whether fish, macroinvertebrates, or bacteria—being considered. For bacterial diversity, we recovered nine abundant operational taxonomic units (OTUs) that comprised a core H2S-rich stream microbiome in the region. Many H2S-associated OTUs were members of the Epsilonproteobacteria and Gammaproteobacteria, which both have been implicated in endosymbiotic relationships between sulfur-oxidizing bacteria and eukaryotes, suggesting the potential for symbioses that remain to be discovered in these habitats.


16S sequencing Microbial ecology Toxicity Sulfur oxidation Biogeography Mexico 



The authors thank Omar Cornejo for the use of his laboratory space and input, Caren Goldberg for microbial sampling advice, Lisa Orfe for sequencing assistance, Joe Giersch for help producing the sampling map, Lydia Zeglin for statistical input, Anthony Brown and Ryan Greenway for assistance in the field, members of the Kelley and Cornejo labs for manuscript comments, and two anonymous reviewers for their input on the manuscript.

Funding Information

Research was supported by grants from the National Science Foundation (IOS-1557860 to M.T.; IOS-1557795 to J.L.K.), US Army Research Office (W911NF-15-1-0175 to M.T. and J.L.K.), NIH COBRE Phase III (P30GM103324), and the Explorers Club Youth Activity Fund Grant to J.B.P.

Supplementary material

248_2018_1237_MOESM1_ESM.docx (3.3 mb)
ESM 1 (DOCX 3363 kb)


  1. 1.
    MacArthur RH, Wilson EO (2016) The theory of island biogeography. Princeton university pressGoogle Scholar
  2. 2.
    Clark DR, Mathieu M, Mourot L, Dufossé L, Underwood GJ, Dumbrell AJ, McGenity TJ (2017) Biogeography at the limits of life: do extremophilic microbial communities show biogeographical regionalization? Glob. Ecol. Biogeogr. 26:1435–1446CrossRefGoogle Scholar
  3. 3.
    Anderson RE, Sogin ML, Baross JA (2014) Biogeography and ecology of the rare and abundant microbial lineages in deep-sea hydrothermal vents. FEMS Microbiol. Ecol. 91:1CrossRefGoogle Scholar
  4. 4.
    Mino S, Nakagawa S, Makita H, Toki T, Miyazaki J, Sievert SM, Polz MF, Inagaki F, Godfroy A, Kato S (2017) Endemicity of the cosmopolitan mesophilic chemolithoautotroph Sulfurimonas at deep-sea hydrothermal vents. The ISME Journal 11:909–919CrossRefGoogle Scholar
  5. 5.
    Fierer N, Morse JL, Berthrong ST, Bernhardt ES, Jackson RB (2007) Environmental controls on the landscape-scale biogeography of stream bacterial communities. Ecology 88:2162–2173CrossRefGoogle Scholar
  6. 6.
    Baas-Becking LGM (1934) Geobiologie; of inleiding tot de milieukunde. WP Van Stockum & Zoon NVGoogle Scholar
  7. 7.
    Rossmassler K, Engel AS, Twing KI, Hanson TE, Campbell BJ (2012) Drivers of epsilonproteobacterial community composition in sulfidic caves and springs. FEMS Microbiol. Ecol. 79:421–432CrossRefGoogle Scholar
  8. 8.
    Headd B, Engel AS (2014) Biogeographic congruency among bacterial communities from terrestrial sulfidic springs. Front. Microbiol. 5:1CrossRefGoogle Scholar
  9. 9.
    Greenway R, Arias-Rodriguez L, Diaz P, Tobler M (2014) Patterns of macroinvertebrate and fish diversity in freshwater sulphide springs. Diversity 6:597–632CrossRefGoogle Scholar
  10. 10.
    Tobler M, Schlupp I, Heubel KU, Riesch R, De León FJG, Giere O, Plath M (2006) Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10:577–585CrossRefGoogle Scholar
  11. 11.
    Headd B, Engel AS (2013) Evidence for niche partitioning revealed by the distribution of sulfur oxidation genes collected from areas of a terrestrial sulfidic spring with differing geochemical conditions. Appl. Environ. Microbiol. 79:1171–1182CrossRefGoogle Scholar
  12. 12.
    Forte E, Giuffrè A (2016) How bacteria breathe in hydrogen sulfide-rich environments. Biochemist 38:8–11Google Scholar
  13. 13.
    Bagarinao T (1992) Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquat. Toxicol. 24:21–62CrossRefGoogle Scholar
  14. 14.
    Hose LD, Palmer AN, Palmer MV, Northup DE, Boston PJ, DuChene HR (2000) Microbiology and geochemistry in a hydrogen-sulphide-rich karst environment. Chem. Geol. 169:399–423CrossRefGoogle Scholar
  15. 15.
    Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr. Opin. Microbiol. 8:253–259CrossRefGoogle Scholar
  16. 16.
    Porter ML, Engel AS (2008) Diversity of uncultured Epsilonproteobacteria from terrestrial sulfidic caves and springs. Appl. Environ. Microbiol. 74:4973–4977CrossRefGoogle Scholar
  17. 17.
    Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile ε-proteobacteria: key players in sulphidic habitats. Nat. Rev. Microbiol. 4:458–468CrossRefGoogle Scholar
  18. 18.
    Waite DW, Vanwonterghem I, Rinke C, Parks DH, Zhang Y, Takai K, Sievert SM, Simon J, Campbell BJ, Hanson TE (2017) Comparative genomic analysis of the class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. nov.). Frontiers in microbiology 8: 682Google Scholar
  19. 19.
    Jørgensen BB, Boetius A (2007) Feast and famine—microbial life in the deep-sea bed. Nat. Rev. Microbiol. 5:770–781CrossRefGoogle Scholar
  20. 20.
    Crump BC, Amaral-Zettler LA, Kling GW (2012) Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils. The ISME Journal 6:1629–1639CrossRefGoogle Scholar
  21. 21.
    Smith DJ, Timonen HJ, Jaffe DA, Griffin DW, Birmele MN, Perry KD, Ward PD, Roberts MS (2013) Intercontinental dispersal of bacteria and archaea by transpacific winds. Appl. Environ. Microbiol. 79:1134–1139CrossRefGoogle Scholar
  22. 22.
    Grossart H-P, Dziallas C, Leunert F, Tang KW (2010) Bacteria dispersal by hitchhiking on zooplankton. Proc. Natl. Acad. Sci. 107:11959–11964CrossRefGoogle Scholar
  23. 23.
    Skirnisdottir S, Hreggvidsson GO, Hjörleifsdottir S, Marteinsson VT, Petursdottir SK, Holst O, Kristjansson JK (2000) Influence of sulfide and temperature on species composition and community structure of hot spring microbial mats. Appl. Environ. Microbiol. 66:2835–2841CrossRefGoogle Scholar
  24. 24.
    Perreault NN, Andersen DT, Pollard WH, Greer CW, Whyte LG (2007) Characterization of the prokaryotic diversity in cold saline perennial springs of the Canadian high Arctic. Appl. Environ. Microbiol. 73:1532–1543CrossRefGoogle Scholar
  25. 25.
    Hotaling S, Hood E, Hamilton TL (2017) Microbial ecology of mountain glacier ecosystems: biodiversity, ecological connections, and implications of a warming climate. Environ. Microbiol. 19:2935–2948. CrossRefGoogle Scholar
  26. 26.
    Tobler M, Palacios M, Chapman LJ, Mitrofanov I, Bierbach D, Plath M, Arias-Rodriguez L, García de León FJ, Mateos M (2011) Evolution in extreme environments: replicated phenotypic differentiation in livebearing fish inhabiting sulfidic springs. Evolution 65:2213–2228CrossRefGoogle Scholar
  27. 27.
    Plath M, Hermann B, Schröder C, Riesch R, Tobler M, de León FJG, Schlupp I, Tiedemann R (2010) Locally adapted fish populations maintain small-scale genetic differentiation despite perturbation by a catastrophic flood event. BMC Evol. Biol. 10:256CrossRefGoogle Scholar
  28. 28.
    Lagarde LR, Boston PJ, Campbell AR, Hose LD, Axen G, Stafford KW (2014) Hydrogeology of northern Sierra de Chiapas, Mexico: a conceptual model based on a geochemical characterization of sulfide-rich karst brackish springs. Hydrogeol. J. 22:1447–1467CrossRefGoogle Scholar
  29. 29.
    Wilhelm L, Singer GA, Fasching C, Battin TJ, Besemer K (2013) Microbial biodiversity in glacier-fed streams. ISME J. 7:1651–1660. CrossRefGoogle Scholar
  30. 30.
    Rosales Lagarde L, Boston P, Campbell A, Stafford K (2006) Possible structural connection between Chichón volcano and the sulfur-rich springs of Villa Luz cave (aka Cueva de las Sardinas), southern Mexico. Assoc Mex Cave Stud Bull 19:177–184Google Scholar
  31. 31.
    Goldberg CS, Pilliod DS, Arkle RS, Waits LP (2011) Molecular detection of vertebrates in stream water: a demonstration using Rocky Mountain tailed frogs and Idaho giant salamanders. PLoS One 6:e22746CrossRefGoogle Scholar
  32. 32.
    Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl. Environ. Microbiol. 74:2461–2470CrossRefGoogle Scholar
  33. 33.
    Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963CrossRefGoogle Scholar
  34. 34.
    Gordon A, Hannon G (2010) Fastx-toolkitGoogle Scholar
  35. 35.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336CrossRefGoogle Scholar
  36. 36.
    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069–5072CrossRefGoogle Scholar
  37. 37.
    Shannon CE, Weaver W (1998) The mathematical theory of communication. University of Illinois pressGoogle Scholar
  38. 38.
    Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community Ecol. Packag 10:631–637Google Scholar
  39. 39.
    Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26:1641–1650CrossRefGoogle Scholar
  40. 40.
    Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33:475–505CrossRefGoogle Scholar
  41. 41.
    Hamilton N (2015) Ggtern: an extension to ggplot2, for the creation of ternary diagrams. R package version 1Google Scholar
  42. 42.
    Lindström ES, Langenheder S (2012) Local and regional factors influencing bacterial community assembly. Environ. Microbiol. Rep. 4:1–9CrossRefGoogle Scholar
  43. 43.
    Hotaling S, Finn DS, Giersch JJ, Weisrock DW, Jacobsen D (2017) Climate change and alpine stream biology: progress, challenges, and opportunities for the future. Biol. Rev 92:2024–2045. CrossRefGoogle Scholar
  44. 44.
    Ward JV (1994) Ecology of alpine streams. Freshw. Biol. 32:277–294CrossRefGoogle Scholar
  45. 45.
    Inskeep WP, Jay ZJ, Tringe SG, Herrgård MJ, Rusch DB, Committee YMPS, Members WG (2013) The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front. Microbiol. 4Google Scholar
  46. 46.
    Findlay S (2010) Stream microbial ecology. J. N. Am. Benthol. Soc. 29:170–181CrossRefGoogle Scholar
  47. 47.
    Bricheux G, Morin L, Moal G, Coffe G, Balestrino D, Charbonnel N, Bohatier J, Forestier C (2013) Pyrosequencing assessment of prokaryotic and eukaryotic diversity in biofilm communities from a French river. Microbiologyopen 2:402–414CrossRefGoogle Scholar
  48. 48.
    Padial AA, Ceschin F, Declerck SA, De Meester L, Bonecker CC, Lansac-Tôha FA, Rodrigues L, Rodrigues LC, Train S, Velho LF (2014) Dispersal ability determines the role of environmental, spatial and temporal drivers of metacommunity structure. PLoS One 9:e111227CrossRefGoogle Scholar
  49. 49.
    Shurin JB, Cottenie K, Hillebrand H (2009) Spatial autocorrelation and dispersal limitation in freshwater organisms. Oecologia 159:151–159CrossRefGoogle Scholar
  50. 50.
    Meier DV, Pjevac P, Bach W, Hourdez S, Girguis PR, Vidoudez C, Amann R, Meyerdierks A (2017) Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents. The ISME Journal 11:1545–1558CrossRefGoogle Scholar
  51. 51.
    Anantharaman K, Breier JA, Sheik CS, Dick GJ (2013) Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc. Natl. Acad. Sci. 110:330–335CrossRefGoogle Scholar
  52. 52.
    Assié A, Borowski C, van der Heijden K, Raggi L, Geier B, Leisch N, Schimak MP, Dubilier N, Petersen JM (2016) A specific and widespread association between deep-sea Bathymodiolus mussels and a novel family of Epsilonproteobacteria. Environ. Microbiol. Rep. 8:805–813CrossRefGoogle Scholar
  53. 53.
    Watanabe T, Kojima H, Fukui M (2014) Complete genomes of freshwater sulfur oxidizers Sulfuricella denitrificans skB26 and Sulfuritalea hydrogenivorans sk43H: genetic insights into the sulfur oxidation pathway of betaproteobacteria. Syst. Appl. Microbiol. 37:387–395CrossRefGoogle Scholar
  54. 54.
    Vésteinsdóttir H, Reynisdóttir DB, Örlygsson J (2011) Thiomonas islandica sp. nov., a moderately thermophilic, hydrogen-and sulfur-oxidizing betaproteobacterium isolated from a hot spring. Int. J. Syst. Evol. Microbiol. 61:132–137CrossRefGoogle Scholar
  55. 55.
    Slobodkin A (2014) The family Peptostreptococcaceae. The prokaryotes. Springer, pp. 291–302Google Scholar
  56. 56.
    Brown L, Wolf JM, Prados-Rosales R, Casadevall A (2015) Through the wall: extracellular vesicles in gram-positive bacteria, mycobacteria and fungi. Nat. Rev. Microbiol. 13:620–630CrossRefGoogle Scholar
  57. 57.
    Bland CS, Ireland JM, Lozano E, Alvarez ME, Primm TP (2005) Mycobacterial ecology of the Rio Grande. Appl. Environ. Microbiol. 71:5719–5727CrossRefGoogle Scholar
  58. 58.
    Mangold S, Valdés J, Holmes D, Dopson M (2011) Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus. Front. Microbiol. 2:17CrossRefGoogle Scholar
  59. 59.
    Sievert SM, Scott KM, Klotz MG, Chain PS, Hauser LJ, Hemp J, Hügler M, Land M, Lapidus A, Larimer FW (2008) Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl. Environ. Microbiol. 74:1145–1156CrossRefGoogle Scholar
  60. 60.
    Chen XG, Geng AL, Yan R, Gould W, Ng YL, Liang D (2004) Isolation and characterization of sulphur-oxidizing Thiomonas sp. and its potential application in biological deodorization. Lett. Appl. Microbiol. 39:495–503CrossRefGoogle Scholar
  61. 61.
    Kodama Y, Watanabe K (2004) Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity. Int. J. Syst. Evol. Microbiol. 54:2297–2300CrossRefGoogle Scholar
  62. 62.
    Engel AS, Porter ML, Stern LA, Quinlan S, Bennett PC (2004) Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic “Epsilonproteobacteria”. FEMS Microbiol. Ecol. 51:31–53CrossRefGoogle Scholar
  63. 63.
    Collado L, Inza I, Guarro J, Figueras MJ (2008) Presence of Arcobacter spp. in environmental waters correlates with high levels of fecal pollution. Environ. Microbiol. 10:1635–1640CrossRefGoogle Scholar
  64. 64.
    Poretsky R, Rodriguez-R LM, Luo C, Tsementzi D, Konstantinidis KT (2014) Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS One 9:e93827CrossRefGoogle Scholar
  65. 65.
    Chernousova E, Gridneva E, Grabovich M, Dubinina G, Akimov V, Rossetti S, Kuever J (2009) Thiothrix caldifontis sp. nov. and Thiothrix lacustris sp. nov., gammaproteobacteria isolated from sulfide springs. Int. J. Syst. Evol. Microbiol. 59:3128–3135CrossRefGoogle Scholar
  66. 66.
    Carveth CJ, Widmer AM, Bonar SA (2006) Comparison of upper thermal tolerances of native and nonnative fish species in Arizona. Trans. Am. Fish. Soc. 135:1433–1440CrossRefGoogle Scholar
  67. 67.
    Timmerman CM, Chapman LJ (2003) The effect of gestational state on oxygen consumption and response to hypoxia in the sailfin molly, Poecilia latipinna. Environ. Biol. Fish 68:293–299CrossRefGoogle Scholar
  68. 68.
    Kelley JL, Arias-Rodriguez L, Martin DP, Yee M-C, Bustamante CD, Tobler M (2016) Mechanisms underlying adaptation to life in hydrogen sulfide-rich environments. Mol. Biol. Evol. 33:1419–1434CrossRefGoogle Scholar
  69. 69.
    Passow CN, Brown AP, Arias-Rodriquez L, Yee MC, Sockell A, Schartl M, Warren WC, Bustamante C, Kelley JL, Tobler M (2017) Complexities of gene expression patterns in natural populations of an extremophile fish (Poecilia mexicana, Poeciliidae). Mol. Ecol. 26:4211–4225CrossRefGoogle Scholar
  70. 70.
    Brown AP, Greenway R, Morgan S, Quackenbush CR, Giordani L, Arias-Rodriguez L, Tobler M, Kelley JL (2017) Genome-scale data reveals that endemic Poecilia populations from small sulfidic springs display no evidence of inbreeding. Mol. Ecol. 26:4920–4934CrossRefGoogle Scholar
  71. 71.
    Roach KA, Tobler M, Winemiller KO (2011) Hydrogen sulfide, bacteria, and fish: a unique, subterranean food chain. Ecology 92:2056–2062CrossRefGoogle Scholar
  72. 72.
    Tobler M, Scharnweber K, Greenway R, Passow CN, Arias-Rodriguez L, García-De-León FJ (2015) Convergent changes in the trophic ecology of extremophile fish along replicated environmental gradients. Freshw. Biol. 60:768–780CrossRefGoogle Scholar
  73. 73.
    Minic Z, Herve G (2004) Biochemical and enzymological aspects of the symbiosis between the deep-sea tubeworm Riftia pachyptila and its bacterial endosymbiont. FEBS J. 271:3093–3102Google Scholar
  74. 74.
    Dattagupta S, Schaperdoth I, Montanari A, Mariani S, Kita N, Valley JW, Macalady JL (2009) A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. The ISME Journal 3:935–943CrossRefGoogle Scholar
  75. 75.
    Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6:725–740CrossRefGoogle Scholar
  76. 76.
    Zbinden M, Marqué L, Gaudron SM, Ravaux J, Léger N, Duperron S (2015) Epsilonproteobacteria as gill epibionts of the hydrothermal vent gastropod Cyathermia naticoides (north East-Pacific rise). Mar. Biol. 162:435–448CrossRefGoogle Scholar
  77. 77.
    Suzuki Y, Sasaki T, Suzuki M, Nogi Y, Miwa T, Takai K, Nealson KH, Horikoshi K (2005) Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. Hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl. Environ. Microbiol. 71:5440–5450CrossRefGoogle Scholar
  78. 78.
    Jacobsen D, Milner AM, Brown LE, Dangles O (2012) Biodiversity under threat in glacier-fed river systems. Nat. Clim. Chang. 2:361–364CrossRefGoogle Scholar
  79. 79.
    Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol. Evol. 27:219–225CrossRefGoogle Scholar
  80. 80.
    Eloe-Fadrosh EA, Paez-Espino D, Jarett J, Dunfield PF, Hedlund BP, Dekas AE, Grasby SE, Brady AL, Dong H, Briggs BR (2016) Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs. Nat. Commun. 7:10476CrossRefGoogle Scholar
  81. 81.
    Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ, Evans PN, Hugenholtz P, Tyson GW (2017) Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat. Microbiol 2:1533–1542CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological SciencesWashington State UniversityPullmanUSA
  2. 2.Institute for Bioinformatics and Evolutionary Studies (IBEST)University of IdahoMoscowUSA
  3. 3.División Académica de Ciencias BiológicasUniversidad Juárez Autónoma de TabascoVillahermosaMexico
  4. 4.Division of BiologyKansas State UniversityManhattanUSA

Personalised recommendations