Home LiteratureArticle Details
PMID: 17334858 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment.

Microbial ecology ·Vol. 53 ·No. 3 ·2007-04-00 ·Pages 371-83

DeSantis TZ, Brodie EL, Moberg JP, Zubieta IX, Piceno YM, Andersen GL

Abstract

Molecular approaches aimed at detection of a broad-range of prokaryotes in the environment routinely rely on classifying heterogeneous 16S rRNA genes amplified by polymerase chain reaction (PCR) using primers with broad specificity. The general method of sampling and categorizing DNA has been to clone then sequence the PCR products. However, the number of clones required to adequately catalog the majority of taxa in a sample is unwieldy. Alternatively, hybridizing target sequences to a universal 16S rRNA gene microarray may provide a more rapid and comprehensive view of prokaryotic community composition. This study investigated the breadth and accuracy of a microarray in detecting diverse 16S rRNA gene sequence types compared to clone-and-sequencing using three environmental samples: urban aerosol, subsurface soil, and subsurface water. PCR products generated from universal 16S rRNA gene-targeted primers were classified by using either the clone-and-sequence method or by hybridization to a novel high-density microarray of 297,851 probes complementary to 842 prokaryotic subfamilies. The three clone libraries comprised 1391 high-quality sequences. Approximately 8% of the clones could not be placed into a known subfamily and were considered novel. The microarray results confirmed the majority of clone-detected subfamilies and additionally demonstrated greater amplicon diversity extending into phyla not observed by the cloning method. Sequences matching operational taxonomic units within the phyla Nitrospira, Planctomycetes, and TM7, which were uniquely detected by the array, were verified with specific primers and subsequent amplicon sequencing. Subfamily richness detected by the array corresponded well with nonparametric richness predictions extrapolated from clone libraries except in the water community where clone-based richness predictions were greatly exceeded. It was concluded that although the microarray is unreliable in identifying novel prokaryotic taxa, it reveals greater diversity in environmental samples than sequencing a typically sized clone library. Furthermore, the microarray allowed samples to be rapidly evaluated with replication, a significant advantage in studies of microbial ecology.

MeSH Terms
Aerosols Bacteria/classification,genetics Base Sequence Biodiversity Cloning, Molecular/methods DNA Primers/chemistry DNA, Bacterial/chemistry Environmental Microbiology Environmental Monitoring/methods Microarray Analysis/methods Molecular Sequence Data Polymerase Chain Reaction RNA, Ribosomal, 16S/genetics Soil Microbiology Water Microbiology
Chemicals
Aerosols DNA Primers DNA, Bacterial RNA, Ribosomal, 16S
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
DeSantis Todd Z
Lawrence Berkeley National Laboratory, Center for Environmental Biotechnology, 1 Cyclotron Road, Mail Stop 70A-3317, Berkeley, CA 94720, USA.
Brodie Eoin L
Moberg Jordan P
Zubieta Ingrid X
Piceno Yvette M
Andersen Gary L
References (56)
56 references, click to expand
  1. Development of a universal microarray based on the ligation detection reaction and 16S rrna gene polymorphism to target diversity of cyanobacteria.
    Appl Environ Microbiol. 2004 Dec;70(12):7161-72 PMID: 15574913
  2. Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale.
    J Microbiol Methods. 2003 Oct;55(1):155-64 PMID: 14500007
  3. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.
    Appl Environ Microbiol. 2006 Jul;72(7):5069-72 PMID: 16820507
  4. ARB: a software environment for sequence data.
    Nucleic Acids Res. 2004 Feb 25;32(4):1363-71 PMID: 14985472
  5. Bias in template-to-product ratios in multitemplate PCR.
    Appl Environ Microbiol. 1998 Oct;64(10):3724-30 PMID: 9758791
  6. Magnetic, microplate-format plasmid isolation protocol for high-yield, sequencing-grade DNA.
    Biotechniques. 2000 Oct;29(4):786-8, 790, 792 PMID: 11056809
  7. Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species.
    Appl Environ Microbiol. 1995 Jul;61(7):2798-801 PMID: 7618894
  8. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes.
    Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W394-9 PMID: 16845035
  9. Development and evaluation of functional gene arrays for detection of selected genes in the environment.
    Appl Environ Microbiol. 2001 Dec;67(12):5780-90 PMID: 11722935
  10. Novel techniques for analysing microbial diversity in natural and perturbed environments.
    J Biotechnol. 1998 Sep 17;64(1):53-62 PMID: 9823658
  11. Empirical and theoretical bacterial diversity in four Arizona soils.
    Appl Environ Microbiol. 2002 Jun;68(6):3035-45 PMID: 12039765
  12. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity.
    J Bacteriol. 1998 Sep;180(18):4765-74 PMID: 9733676
  13. Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy patients.
    J Clin Microbiol. 2003 Feb;41(2):558-63 PMID: 12574246
  14. Simultaneous discrimination between 15 fish pathogens by using 16S ribosomal DNA PCR and DNA microarrays.
    Appl Environ Microbiol. 2004 Jul;70(7):4216-21 PMID: 15240304
  15. Comprehensive aligned sequence construction for automated design of effective probes (CASCADE-P) using 16S rDNA.
    Bioinformatics. 2003 Aug 12;19(12):1461-8 PMID: 12912825
  16. Sequence-specific identification of 18 pathogenic microorganisms using microarray technology.
    Mol Cell Probes. 2002 Apr;16(2):119-27 PMID: 12030762
  17. Rapid quantification and taxonomic classification of environmental DNA from both prokaryotic and eukaryotic origins using a microarray.
    FEMS Microbiol Lett. 2005 Apr 15;245(2):271-8 PMID: 15837382
  18. Microarrays for bacterial detection and microbial community analysis.
    Curr Opin Microbiol. 2003 Jun;6(3):288-94 PMID: 12831906
  19. Taking arrays from the lab to the field: trying to make sense of the unknown.
    Biotechniques. 2005 Apr;38(4):591-600 PMID: 15884677
  20. Oligonucleotide microarray for identification of Enterococcus species.
    FEMS Microbiol Lett. 2005 May 1;246(1):133-42 PMID: 15869972
  21. Directional cDNA library construction assisted by the in vitro recombination reaction.
    Nucleic Acids Res. 2001 Feb 15;29(4):E22 PMID: 11160942
  22. Base-calling of automated sequencer traces using phred. II. Error probabilities.
    Genome Res. 1998 Mar;8(3):186-94 PMID: 9521922
  23. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness.
    Appl Environ Microbiol. 2005 Mar;71(3):1501-6 PMID: 15746353
  24. Improved assessment of denitrifying, N2-fixing, and total-community bacteria by terminal restriction fragment length polymorphism analysis using multiple restriction enzymes.
    Appl Environ Microbiol. 2005 Apr;71(4):2026-35 PMID: 15812035
  25. Chimeric 16S rDNA sequences of diverse origin are accumulating in the public databases.
    Int J Syst Evol Microbiol. 2003 Jan;53(Pt 1):289-93 PMID: 12656186
  26. High-density microarray of small-subunit ribosomal DNA probes.
    Appl Environ Microbiol. 2002 May;68(5):2535-41 PMID: 11976131
  27. Novel major bacterial candidate division within a municipal anaerobic sludge digester.
    Appl Environ Microbiol. 2005 Apr;71(4):2145-53 PMID: 15812049
  28. Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments.
    Appl Environ Microbiol. 2002 May;68(5):2300-6 PMID: 11976101
  29. Prominent occurrence of ribosomes from an uncultured bacterium of the Verrucomicrobiales cluster in grassland soils.
    Lett Appl Microbiol. 1998 Mar;26(3):219-23 PMID: 9569713
  30. Functional gene diversity analysis in BTEX contaminated soils by means of PCR-SSCP DNA fingerprinting: comparative diversity assessment against bacterial isolates and PCR-DNA clone libraries.
    Environ Microbiol. 2004 Feb;6(2):95-110 PMID: 14756875
  31. An orthogonal oligonucleotide protecting group strategy that enables assembly of repetitive or highly structured DNAs.
    Nucleic Acids Res. 2002 Oct 1;30(19):e101 PMID: 12364618
  32. Identification of polyphosphate-accumulating organisms and design of 16S rRNA-directed probes for their detection and quantitation.
    Appl Environ Microbiol. 2000 Mar;66(3):1175-82 PMID: 10698788
  33. Archaeal population dynamics during sequential reduction processes in rice field soil.
    Appl Environ Microbiol. 2000 Jul;66(7):2732-42 PMID: 10877762
  34. Accessing genetic information with high-density DNA arrays.
    Science. 1996 Oct 25;274(5287):610-4 PMID: 8849452
  35. Investigation of candidate division TM7, a recently recognized major lineage of the domain Bacteria with no known pure-culture representatives.
    Appl Environ Microbiol. 2001 Jan;67(1):411-9 PMID: 11133473
  36. Use of stable-isotope probing, full-cycle rRNA analysis, and fluorescence in situ hybridization-microautoradiography to study a methanol-fed denitrifying microbial community.
    Appl Environ Microbiol. 2004 Jan;70(1):588-96 PMID: 14711691
  37. Reoxidation of bioreduced uranium under reducing conditions.
    Environ Sci Technol. 2005 Aug 15;39(16):6162-9 PMID: 16173577
  38. Escherichia coli gene expression responsive to levels of the response regulator EvgA.
    J Bacteriol. 2002 Nov;184(22):6225-34 PMID: 12399493
  39. Single-base-pair discrimination of terminal mismatches by using oligonucleotide microarrays and neural network analyses.
    Appl Environ Microbiol. 2002 Jan;68(1):235-44 PMID: 11772632
  40. Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring.
    Appl Environ Microbiol. 2003 Sep;69(9):5609-21 PMID: 12957951
  41. DNA microarray detection of nitrifying bacterial 16S rRNA in wastewater treatment plant samples.
    Water Res. 2005 Sep;39(14):3229-38 PMID: 16009395
  42. Enumeration of total bacteria and bacteria with genes for proteolytic activity in pure cultures and in environmental samples by quantitative PCR mediated amplification.
    J Microbiol Methods. 2002 May;49(3):235-45 PMID: 11869788
  43. Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures.
    Appl Environ Microbiol. 1999 Apr;65(4):1721-30 PMID: 10103273
  44. Primer3 on the WWW for general users and for biologist programmers.
    Methods Mol Biol. 2000;132:365-86 PMID: 10547847
  45. Amplification of bacterial 16S ribosomal DNA with polymerase chain reaction.
    J Clin Microbiol. 1990 Sep;28(9):1942-6 PMID: 2095137
  46. Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples.
    Appl Environ Microbiol. 1999 Nov;65(11):4715-24 PMID: 10543776
  47. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments.
    Bioinformatics. 2004 Sep 22;20(14):2317-9 PMID: 15073015
  48. Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing.
    J Bacteriol. 1991 Jul;173(14):4371-8 PMID: 2066334
  49. Computational improvements reveal great bacterial diversity and high metal toxicity in soil.
    Science. 2005 Aug 26;309(5739):1387-90 PMID: 16123304
  50. Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities.
    Appl Environ Microbiol. 2003 Nov;69(11):6768-76 PMID: 14602639
  51. Genetic relatedness of Legionella longbeachae isolates from human and environmental sources in Australia.
    Appl Environ Microbiol. 1990 Sep;56(9):2784-90 PMID: 1980403
  52. Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation.
    Appl Environ Microbiol. 1998 Oct;64(10):3869-77 PMID: 9758812
  53. Base-calling of automated sequencer traces using phred. I. Accuracy assessment.
    Genome Res. 1998 Mar;8(3):175-85 PMID: 9521921
  54. Counting the uncountable: statistical approaches to estimating microbial diversity.
    Appl Environ Microbiol. 2001 Oct;67(10):4399-406 PMID: 11571135
  55. Status of the microbial census.
    Microbiol Mol Biol Rev. 2004 Dec;68(4):686-91 PMID: 15590780
  56. Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment.
    Appl Environ Microbiol. 2002 Oct;68(10):5064-81 PMID: 12324358
Article Info
Journal
Microbial ecology
Abbr.
Microb Ecol
ISSN
0095-3628
DOI
10.1007/s00248-006-9134-9
Published
2007-04-00
Epub
2007-00-02
Pages
371-83
Language
English
Region
United States
NLM ID
7500663
Subset
IM
Databases
GENBANK
DQ125500, DQ125501, DQ125502, DQ125503, DQ125504, DQ125505, DQ125506, DQ125507, DQ125508, DQ125509, DQ125510, DQ125511, DQ125512, DQ125513, DQ125514, DQ125515, DQ125516, DQ125517, DQ125518, DQ125519, DQ125520, DQ125521, DQ125522, DQ125523, DQ125524, DQ125525, DQ125526, DQ125527, DQ125528, DQ125529, DQ125530, DQ125531, DQ125532, DQ125533, DQ125534, DQ125535, DQ125536, DQ125537, DQ125538, DQ125539, DQ125540, DQ125541, DQ125542, DQ125543, DQ125544, DQ125545, DQ125546, DQ125547, DQ125548, DQ125549, DQ125550, DQ125551, DQ125552, DQ125553, DQ125554, DQ125555, DQ125556, DQ125557, DQ125558, DQ125559, DQ125560, DQ125561, DQ125562, DQ125563, DQ125564, DQ125565, DQ125566, DQ125567, DQ125568, DQ125569, DQ125570, DQ125571, DQ125572, DQ125573, DQ125574, DQ125575, DQ125576, DQ125577, DQ125578, DQ125579, DQ125580, DQ125581, DQ125582, DQ125583, DQ125584, DQ125585, DQ125586, DQ125587, DQ125588, DQ125589, DQ125590, DQ125591, DQ125592, DQ125593, DQ125594, DQ125595, DQ125596, DQ125597, DQ125598, DQ125599, DQ125600, DQ125601, DQ125602, DQ125603, DQ125604, DQ125605, DQ125606, DQ125607, DQ125608, DQ125609, DQ125610, DQ125611, DQ125612, DQ125613, DQ125614, DQ125615, DQ125616, DQ125617, DQ125618, DQ125619, DQ125620, DQ125621, DQ125622, DQ125623, DQ125624, DQ125625, DQ125626, DQ125627, DQ125628, DQ125629, DQ125630, DQ125631, DQ125632, DQ125633, DQ125634, DQ125635, DQ125636, DQ125637, DQ125638, DQ125639, DQ125640, DQ125641, DQ125642, DQ125643, DQ125644, DQ125645, DQ125646, DQ125647, DQ125648, DQ125649, DQ125650, DQ125651, DQ125652, DQ125653, DQ125654, DQ125655, DQ125656, DQ125657, DQ125658, DQ125659, DQ125660, DQ125661, DQ125662, DQ125663, DQ125664, DQ125665, DQ125666, DQ125667, DQ125668, DQ125669, DQ125670, DQ125671, DQ125672, DQ125673, DQ125674, DQ125675, DQ125676, DQ125677, DQ125678, DQ125679, DQ125680, DQ125681, DQ125682, DQ125683, DQ125684, DQ125685, DQ125686, DQ125687, DQ125688, DQ125689, DQ125690, DQ125691, DQ125692, DQ125693, DQ125694, DQ125695, DQ125696, DQ125697, DQ125698, DQ125699, DQ125700, DQ125701, DQ125702, DQ125703, DQ125704, DQ125705, DQ125706, DQ125707, DQ125708, DQ125709, DQ125710, DQ125711, DQ125712, DQ125713, DQ125714, DQ125715, DQ125716, DQ125717, DQ125718, DQ125719, DQ125720, DQ125721, DQ125722, DQ125723, DQ125724, DQ125725, DQ125726, DQ125727, DQ125728, DQ125729, DQ125730, DQ125731, DQ125732, DQ125733, DQ125734, DQ125735, DQ125736, DQ125737, DQ125738, DQ125739, DQ125740, DQ125741, DQ125742, DQ125743, DQ125744, DQ125745, DQ125746, DQ125747, DQ125748, DQ125749, DQ125750, DQ125751, DQ125752, DQ125753, DQ125754, DQ125755, DQ125756, DQ125757, DQ125758, DQ125759, DQ125760, DQ125761, DQ125762, DQ125763, DQ125764, DQ125765, DQ125766, DQ125767, DQ125768, DQ125769, DQ125770, DQ125771, DQ125772, DQ125773, DQ125774, DQ125775, DQ125776, DQ125777, DQ125778, DQ125779, DQ125780, DQ125781, DQ125782, DQ125783, DQ125784, DQ125785, DQ125786, DQ125787, DQ125788, DQ125789, DQ125790, DQ125791, DQ125792, DQ125793, DQ125794, DQ125795, DQ125796, DQ125797, DQ125798, DQ125799, DQ125800, DQ125801, DQ125802, DQ125803, DQ125804, DQ125805, DQ125806, DQ125807, DQ125808, DQ125809, DQ125810, DQ125811, DQ125812, DQ125813, DQ125814, DQ125815, DQ125816, DQ125817, DQ125818, DQ125819, DQ125820, DQ125821, DQ125822, DQ125823, DQ125824, DQ125825, DQ125826, DQ125827, DQ125828, DQ125829, DQ125830, DQ125831, DQ125832, DQ125833, DQ125834, DQ125835, DQ125836, DQ125837, DQ125838, DQ125839, DQ125840, DQ125841, DQ125842, DQ125843, DQ125844, DQ125845, DQ125846, DQ125847, DQ125848, DQ125849, DQ125850, DQ125851, DQ125852, DQ125853, DQ125854, DQ125855, DQ125856, DQ125857, DQ125858, DQ125859, DQ125860, DQ125861, DQ125862, DQ125863, DQ125864, DQ125865, DQ125866, DQ125867, DQ125868, DQ125869, DQ125870, DQ125871, DQ125872, DQ125873, DQ125874, DQ125875, DQ125876, DQ125877, DQ125878, DQ125879, DQ125880, DQ125881, DQ125882, DQ125883, DQ125884, DQ125885, DQ125886, DQ125887, DQ125888, DQ125889, DQ125890, DQ125891, DQ125892, DQ125893, DQ125894, DQ125895, DQ125896, DQ125897, DQ125898, DQ125899, DQ125900, DQ125901, DQ125902, DQ125903, DQ125904, DQ125905, DQ125906, DQ125907, DQ125908, DQ125909, DQ125910, DQ125911, DQ125912, DQ125913, DQ125914, DQ125915, DQ125916, DQ125917, DQ125918, DQ125919, DQ125920, DQ125921, DQ125922, DQ125923, DQ125924, DQ125925, DQ125926, DQ125927, DQ125928, DQ125929, DQ125930, DQ125931, DQ125932, DQ125933, DQ125934, DQ125935, DQ129237, DQ129238, DQ129239, DQ129240, DQ129241, DQ129242, DQ129243, DQ129244, DQ129245, DQ129246, DQ129247, DQ129248, DQ129249, DQ129250, DQ129251, DQ129252, DQ129253, DQ129254, DQ129255, DQ129256, DQ129257, DQ129258, DQ129259, DQ129260, DQ129261, DQ129262, DQ129263, DQ129264, DQ129265, DQ129266, DQ129267, DQ129268, DQ129269, DQ129270, DQ129271, DQ129272, DQ129273, DQ129274, DQ129275, DQ129276, DQ129277, DQ129278, DQ129279, DQ129280, DQ129281, DQ129282, DQ129283, DQ129284, DQ129285, DQ129286, DQ129287, DQ129288, DQ129289, DQ129290, DQ129291, DQ129292, DQ129293, DQ129294, DQ129295, DQ129296, DQ129297, DQ129298, DQ129299, DQ129300, DQ129301, DQ129302, DQ129303, DQ129304, DQ129305, DQ129306, DQ129307, DQ129308, DQ129309, DQ129310, DQ129311, DQ129312, DQ129313, DQ129314, DQ129315, DQ129316, DQ129317, DQ129318, DQ129319, DQ129320, DQ129321, DQ129322, DQ129323, DQ129324, DQ129325, DQ129326, DQ129327, DQ129328, DQ129329, DQ129330, DQ129331, DQ129332, DQ129333, DQ129334, DQ129335, DQ129336, DQ129337, DQ129338, DQ129339, DQ129340, DQ129341, DQ129342, DQ129343, DQ129344, DQ129345, DQ129346, DQ129347, DQ129348, DQ129349, DQ129350, DQ129351, DQ129352, DQ129353, DQ129354, DQ129355, DQ129356, DQ129357, DQ129358, DQ129359, DQ129360, DQ129361, DQ129362, DQ129363, DQ129364, DQ129365, DQ129366, DQ129367, DQ129368, DQ129369, DQ129370, DQ129371, DQ129372, DQ129373, DQ129374, DQ129375, DQ129376, DQ129377, DQ129378, DQ129379, DQ129380, DQ129381, DQ129382, DQ129383, DQ129384, DQ129385, DQ129386, DQ129387, DQ129388, DQ129389, DQ129390, DQ129391, DQ129392, DQ129393, DQ129394, DQ129395, DQ129396, DQ129397, DQ129398, DQ129399, DQ129400, DQ129401, DQ129402, DQ129403, DQ129404, DQ129405, DQ129406, DQ129407, DQ129408, DQ129409, DQ129410, DQ129411, DQ129412, DQ129413, DQ129414, DQ129415, DQ129416, DQ129417, DQ129418, DQ129419, DQ129420, DQ129421, DQ129422, DQ129423, DQ129424, DQ129425, DQ129426, DQ129427, DQ129428, DQ129429, DQ129430, DQ129431, DQ129432, DQ129433, DQ129434, DQ129435, DQ129436, DQ129437, DQ129438, DQ129439, DQ129440, DQ129441, DQ129442, DQ129443, DQ129444, DQ129445, DQ129446, DQ129447, DQ129448, DQ129449, DQ129450, DQ129451, DQ129452, DQ129453, DQ129454, DQ129455, DQ129456, DQ129457, DQ129458, DQ129459, DQ129460, DQ129461, DQ129462, DQ129463, DQ129464, DQ129465, DQ129466, DQ129467, DQ129468, DQ129469, DQ129470, DQ129471, DQ129472, DQ129473, DQ129474, DQ129475, DQ129476, DQ129477, DQ129478, DQ129479, DQ129480, DQ129481, DQ129482, DQ129483, DQ129484, DQ129485, DQ129486, DQ129487, DQ129488, DQ129489, DQ129490, DQ129491, DQ129492, DQ129493, DQ129494, DQ129495, DQ129496, DQ129497, DQ129498, DQ129499, DQ129500, DQ129501, DQ129502, DQ129503, DQ129504, DQ129505, DQ129506, DQ129507, DQ129508, DQ129509, DQ129510, DQ129511, DQ129512, DQ129513, DQ129514, DQ129515, DQ129516, DQ129517, DQ129518, DQ129519, DQ129520, DQ129521, DQ129522, DQ129523, DQ129524, DQ129525, DQ129526, DQ129527, DQ129528, DQ129529, DQ129530, DQ129531, DQ129532, DQ129533, DQ129534, DQ129535, DQ129536, DQ129537, DQ129538, DQ129539, DQ129540, DQ129541, DQ129542, DQ129543, DQ129544, DQ129545, DQ129546, DQ129547, DQ129548, DQ129549, DQ129550, DQ129551, DQ129552, DQ129553, DQ129554, DQ129555, DQ129556, DQ129557, DQ129558, DQ129559, DQ129560, DQ129561, DQ129562, DQ129563, DQ129564, DQ129565, DQ129566, DQ129567, DQ129568, DQ129569, DQ129570, DQ129571, DQ129572, DQ129573, DQ129574, DQ129575, DQ129576, DQ129577, DQ129578, DQ129579, DQ129580, DQ129581, DQ129582, DQ129583, DQ129584, DQ129585, DQ129586, DQ129587, DQ129588, DQ129589, DQ129590, DQ129591, DQ129592, DQ129593, DQ129594, DQ129595, DQ129596, DQ129597, DQ129598, DQ129599, DQ129600, DQ129601, DQ129602, DQ129603, DQ129604, DQ129605, DQ129606, DQ129607, DQ129608, DQ129609, DQ129610, DQ129611, DQ129612, DQ129613, DQ129614, DQ129615, DQ129616, DQ129617, DQ129618, DQ129619, DQ129620, DQ129621, DQ129622, DQ129623, DQ129624, DQ129625, DQ129626, DQ129627, DQ129628, DQ129629, DQ129630, DQ129631, DQ129632, DQ129633, DQ129634, DQ129635, DQ129636, DQ129637, DQ129638, DQ129639, DQ129640, DQ129641, DQ129642, DQ129643, DQ129644, DQ129645, DQ129646, DQ129647, DQ129648, DQ129649, DQ129650, DQ129651, DQ129652, DQ129653, DQ129654, DQ129655, DQ129656, DQ264398, DQ264399, DQ264400, DQ264401, DQ264402, DQ264403, DQ264404, DQ264405, DQ264406, DQ264407, DQ264408, DQ264409, DQ264410, DQ264411, DQ264412, DQ264413, DQ264414, DQ264415, DQ264416, DQ264417, DQ264418, DQ264419, DQ264420, DQ264421, DQ264422, DQ264423, DQ264424, DQ264425, DQ264426, DQ264427, DQ264428, DQ264429, DQ264430, DQ264431, DQ264432, DQ264433, DQ264434, DQ264435, DQ264436, DQ264437, DQ264438, DQ264439, DQ264440, DQ264441, DQ264442, DQ264443, DQ264444, DQ264445, DQ264446, DQ264447, DQ264448, DQ264449, DQ264450, DQ264451, DQ264452, DQ264453, DQ264454, DQ264455, DQ264456, DQ264457, DQ264458, DQ264459, DQ264460, DQ264461, DQ264462, DQ264463, DQ264464, DQ264465, DQ264466, DQ264467, DQ264468, DQ264469, DQ264470, DQ264471, DQ264472, DQ264473, DQ264474, DQ264475, DQ264476, DQ264477, DQ264478, DQ264479, DQ264480, DQ264481, DQ264482, DQ264483, DQ264484, DQ264485, DQ264486, DQ264487, DQ264488, DQ264489, DQ264490, DQ264491, DQ264492, DQ264493, DQ264494, DQ264495, DQ264496, DQ264497, DQ264498, DQ264499, DQ264500, DQ264501, DQ264502, DQ264503, DQ264504, DQ264505, DQ264506, DQ264507, DQ264508, DQ264509, DQ264510, DQ264511, DQ264512, DQ264513, DQ264514, DQ264515, DQ264516, DQ264517, DQ264518, DQ264519, DQ264520, DQ264521, DQ264522, DQ264523, DQ264524, DQ264525, DQ264526, DQ264527, DQ264528, DQ264529, DQ264530, DQ264531, DQ264532, DQ264533, DQ264534, DQ264535, DQ264536, DQ264537, DQ264538, DQ264539, DQ264540, DQ264541
External Links
PubMed source DOI: 10.1007/s00248-006-9134-9 View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2