Seasonal diversity of planktonic protists in Southwestern Alberta rivers over a 1-year period as revealed by terminal restriction fragment length polymorphism and 18S rRNA gene library analyses

Applied and Environmental Microbiology

Volumn 78, Issue 16, 2012, Pages 5653-5660

  Thomas, Matthew C ^a,b   Selinger, L Brent ^b   Inglis, G Douglas ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

18S RRNA; ALBERTA; AMPLICONS; CLONE LIBRARY; COMMUNITY STRUCTURES; GEOGRAPHICAL LOCATIONS; NON-METRIC MULTIDIMENSIONAL SCALING; PROTISTAN COMMUNITIES; RIVER BASINS; RIVER WATER; SANGER SEQUENCING; SEASONAL DIFFERENCES; SEASONAL SHIFTS; TEMPORAL DYNAMICS; TERMINAL RESTRICTION FRAGMENT LENGTH POLYMORPHISMS;

CLONING; GENES; RNA; SOCIAL SCIENCES;

RIVERS;

FUNGAL DNA; FUNGAL RNA; PROTOZOAL DNA; PROTOZOAL RNA; RIBOSOME DNA; RNA 18S;

CLONE; COMMUNITY STRUCTURE; FUNGUS; POLYMORPHISM; PROTIST; RIVER WATER; SEASONAL VARIATION; SPECIES DIVERSITY;

ARTICLE; BIODIVERSITY; BIOTA; CANADA; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RIVER; RNA GENE; SEASON;

ALBERTA; BIODIVERSITY; BIOTA; CLUSTER ANALYSIS; DNA, FUNGAL; DNA, PROTOZOAN; DNA, RIBOSOMAL; GENES, RRNA; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RIVERS; RNA, FUNGAL; RNA, PROTOZOAN; RNA, RIBOSOMAL, 18S; SEASONS; SEQUENCE ANALYSIS, DNA;

ALBERT; CANADA; NEW BRUNSWICK;

ALVEOLATA; CENTROHELIOZOA; EUGLENOZOA; FUNGI; PROTISTA; PROTOZOA; VIRIDIPLANTAE;

EID: 84866157088     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00237-12     Document Type: Article

References (73)

1. Abd H, Saeed A, Weintraub A, Sandstrom G. 2009. Vibrio cholerae O139 requires neither capsule nor LPS O side chain to grow inside Acanthamoeba castellanii. J. Med. Microbiol.. 58: 125-131.
2. Abdo Z, et al. 2006. Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ. Microbiol.. 8: 929-938.
3. Abu Kwaik Y, Gao L-Y, Stone BJ, Venkataraman C, Harb OS. 1998. Invasion of protozoa by Legionella pneumophila and its role in bacterial ecology and pathogenesis. Appl. Environ. Microbiol.. 64: 3127-3133.
4. Adiba S, Nizak C, van Baalen M, Denamur E, Depaulis F. 2010. From grazing resistance to pathogenesis: the coincidental evolution of virulence factors. PLoS One 5:e11882. doi:10.1371/journal.pone.0011882.
5. Adl SM, et al. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol.. 52: 399-451.
6. Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM. 2009. A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One 4:e6372. doi:10.1371/journal.pone.0006372.
7. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ. 2005. At least 1 in 20 16S rRNA sequence records currently held in public repos- itories is estimated to contain substantial anomalies. Appl. Environ. Microbiol.. 71: 7724-7736.
8. Axelsson-Olsson D, Waldenstrom J, Broman T, Olsen B, Holmberg M. 2005. Protozoan Acanthamoeba polyphaga as a potential reservoir for Campylobacter jejuni. Appl. Environ. Microbiol.. 71: 987-992.
9. Bailly J, et al. 2007. Soil eukaryotic functional diversity, a metatranscrip- tomic approach. ISME J.. 1: 632-642.
10. Blackshaw RE. 1991. Hairy nightshade (Solanum sarrachoides) interference in dry beans (Phaseolus vulgaris). Weed Sci.. 39: 48-53.
11. Brinkman NE, et al. 2003. Evaluation of a rapid, quantitative real-time PCR method for enumeration of pathogenic Candida cells in water. Appl. Environ. Microbiol.. 69: 1775-1782.
12. Brown MRW, Barker J. 1999. Unexplored reservoirs of pathogenic bacteria: protozoa and biofilms. Trends Microbiol.. 7: 46-50.
13. Bru D, Martin-Laurent F, Philippot L. 2008. Quantification of the detrimental effect of a single primer-template mismatch by real-time PCR using the 16S rRNA gene as an example. Appl. Environ. Microbiol.. 74: 1660-1663.
14. Carrias JF, Amblard C, Bourdier G. 1996. Protistan bacterivory in an oligomesotrophic lake: importance of attached ciliates and flagellates. Microb. Ecol.. 31: 249-268.
15. Casamayor EO, et al. 2002. Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic finger-printing methods in a multipond solar saltern. Environ. Microbiol.. 4: 338-348.
16. Cavalier-Smith T, von der Heyden S. 2007. Molecular phylogeny, scale evolution and taxonomy of centrohelid heliozoa. Mol. Phylogenet. Evol.. 44: 1186-1203.
17. Costa E, Puhl NJ, Selinger LB, Inglis GD. 2009. Characterization of mucosa-associated bacterial communities of the mouse intestine by terminal restriction fragment length polymorphism: utility of sampling strategies and methods to reduce single-stranded DNA artifacts. J. Microbiol. Methods. 78: 175-180.
18. Creer S. 2010. Second-generation sequencing derived insights into the temporal biodiversity dynamics of freshwater protists. Mol. Ecol. 19: 2829-2831.
19. Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH. 2009. T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10:171. doi:10.1186/1471-2105-10-171.
20. Diez B, Pedros-Alio C, Marsh TL, Massana R. 2001. Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl. Environ. Microbiol.. 67: 2942-2951.
21. Diez B, Pedros-Alio C, Massana R. 2001. Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl. Environ. Microbiol.. 67: 2932-2941.
22. Edgcomb V, et al. 2011. Protistan microbial observatory in the Cariaco Basin, Caribbean. I. Pyrosequencing vs Sanger insights into species richness. ISME J.. 5: 1344-1356.
23. Edgcomb VP, Kysela DT, Teske A, de Vera Gomez A, Sogin ML. 2002. Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc. Natl. Acad. Sci. U. S. A.. 99: 7658-7662.
24. Egert M, Friedrich MW. 2003. Formation of pseudo-terminal restriction fragments, a PCR-related bias affecting terminal restriction fragment length polymorphism analysis of microbial community structure. Appl. Environ. Microbiol.. 69: 2555-2562.
25. Egert M, Friedrich MW. 2005. Post-amplification Klenow fragment treatment alleviates PCR bias caused by partially single-stranded amplicons. J. Microbiol. Methods. 61: 69-75.
26. Foissner W. 1999. Protist diversity: estimates of the near-imponderable. Protist. 150: 363-368.
27. Foissner W. 2008. Protist diversity and distribution: some basic considerations. Biodivers. Conserv.. 17: 235-242.
28. Fortunato CS, Herfort L, Zuber P, Baptista AM, Crump BC. 2012. Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient. ISME J.. 6: 554-563.
29. Frost JA. 2001. Current epidemiological issues in human campylobacteriosis. J. Appl. Microbiol. 90:85S-95S. doi:10.1046/j.1365-2672.2001.01357.x.
30. Gannon JJ, Busse MK. 1989. E. coli and enterococci levels in urban stormwater, river water and chlorinated treatment plant effluent. Water Res.. 23: 1167-1176.
31. Gardner TJ, et al. 2011. Outbreak of campylobacteriosis associated with consumption of raw peas. Clin. Infect. Dis.. 53: 26-32.
32. González JM, Iriberri J, Egea L, Barcina I. 1990. Differential rates of digestion of bacteria by freshwater and marine phagotrophic protozoa. Appl. Environ. Microbiol.. 56: 1851-1857.
33. Hamady M, Lozupone C, Knight R. 2010. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J.. 4: 17-27.
34. Huber T, Faulkner G, Hugenholtz P. 2004. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics. 20: 2317-2319.
35. Huws SA, McBain AJ, Gilbert P. 2005. Protozoan grazing and its impact upon population dynamics in biofilm communities. J. Appl. Microbiol.. 98: 238-244.
36. Inglis GD, Boras VF, Houde A. 2011. Enteric campylobacteria and RNA viruses associated with healthy and diarrheic humans in the Chinook Health Region of Southwestern Alberta, Canada. J. Clin. Microbiol.. 49: 209-219.
37. Jöhnk KD, et al. 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Change Biol.. 14: 495-512.
38. Kaplan CW, Kitts CL. 2003. Variation between observed and true terminal restriction fragment length is dependent on true TRF length and pu- rine content. J. Microbiol. Methods. 54: 121-125.
39. Kim E, Wilcox L, Graham L, Graham J. 2004. Genetically distinct populations of the dinoflagellate Peridinium limbatum in neighboring northern Wisconsin lakes. Microb. Ecol.. 48: 521-527.
40. King CH, Shotts EB, Jr, Wooley RE, Porter KG. 1988. Survival of coliforms and bacterial pathogens within protozoa during chlorination. Appl. Environ. Microbiol.. 54: 3023-3033.
41. Kiss ÁK, Ács E, Kiss KT, Török JK. 2009. Structure and seasonal dynamics of the protozoan community (heterotrophic flagellates, ciliates, amoeboid protozoa) in the plankton of a large river (River Danube, Hungary). Eur. J. Protistol.. 45: 121-138.
42. Kopylov A, Kosolapov D. 2011. The structure of the planktic microbial community in the lower reaches of the Ob River near Salekhard. Contemp. Probl. Ecol.. 4: 1-7.
43. Li L-Y, et al. 2011. Diversity and distribution of planktonic protists in the northern South China Sea. J. Plankton Res.. 33: 445-456.
44. Logares R, et al. 2007. Phenotypically different microalgal morphospecies with identical ribosomal DNA: a case of rapid adaptive evolution? Microb. Ecol.. 53: 549-561.
45. Mardis ER. 2008. The impact of next-generation sequencing technology on genetics. Trends Genet.. 24: 133-141.
46. McCune B, Grace JB. 2003. Analysis of ecological communities. MjM Software Design, Gleneden Beach, OR.
47. Molmeret M, Bitar DM, Han L, Kwaik YA. 2004. Disruption of the phagosomal membrane and egress of Legionella pneumophila into the cytoplasm during the last stages of intracellular infection of macrophages and Acanthamoeba polyphaga. Infect. Immun.. 72: 4040-4051.
48. Nolte V, et al. 2010. Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol. Ecol.. 19: 2908-2915.
49. Not F, del Campo J, Balagué V, de Vargas C, Massana R. 2009. New insights into the diversity of marine picoeukaryotes. PLoS One 4:e7143. doi:10.1371/journal.pone.0007143.
50. O'Brien MC, Bolton WE. 1995. Comparison of cell viability probes compatible with fixation and permeabilization for combined surface and intracellular staining in flow cytometry. Cytometry. 19: 243-255.
51. Olsen SJ, et al. 2001. An outbreak of Campylobacter jejuni infections associated with food handler contamination: the use of pulsed-field gel electrophoresis. J. Infect. Dis.. 183: 164-167.
52. Pearson AD, et al. 2000. Continuous source outbreak of campylobacteriosis traced to chicken. J. Food Prot.. 63: 309-314.
53. Pebody RG, Ryan MJ, Wall PG. 1997. Outbreaks of Campylobacter infection: rare events for a common pathogen. Commun. Dis. Rep. CDR Rev. 7:R33-R37.
54. Pernthaler J. 2005. Predation on prokaryotes in the water column and its ecological implications. Nat. Rev. Microbiol.. 3: 537-546.
55. Ploug H, Stolte W, Epping EHG, Jorgensen BB. 1999. Diffusive boundary layers, photosynthesis, and respiration of the colony-forming plankton algae, Phaeocystis sp. Limnol. Oceanogr.. 44: 1949-1958.
56. Polz MF, Cavanaugh CM. 1998. Bias in template-to-product ratios in multitemplate PCR. Appl. Environ. Microbiol.. 64: 3724-3730.
57. Pruesse E, et al. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res.. 35: 7188-7196.
58. Rawsthorne H, Phister TG. 2009. The presence of Saccharomyces cerevisiae DNA in various media used to propagate yeasts and its removal by ethidium monoazide. Lett. Appl. Microbiol.. 49: 652-654.
59. Ribblett SG, Palmer MA, Coats DW. 2005. The importance of bacterivorous protists in the decomposition of stream leaf litter. Freshw. Biol.. 50: 516-526.
60. Rudi K, Moen B, Dromtorp SM, Holck AL. 2005. Use of ethidium monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Appl. Environ. Microbiol.. 71: 1018-1024.
61. Russell AG, Schnare MN, Gray MW. 2004. Pseudouridine-guide RNAs and other Cbf5p-associated RNAs in Euglena gracilis. RNA. 10: 1034-1046.
62. Salmanian A-H, et al. 2012. Foodborne yeasts serve as reservoirs of Helicobacter pylori. J. Food Saf.. 32: 152-160.
63. Sandström G, Saeed A, Abd H. 2010. Acanthamoeba polyphaga is a possible host for Vibrio cholerae in aquatic environments. Exp. Parasitol.. 126: 65-68.
64. Schloss PD, et al. 2009. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol.. 75: 7537-7541.
65. Shi X, Liu X, Liu G, Sun Z, Xu H. 2012. An approach to analyzing spatial patterns of protozoan communities for assessing water quality in the Hangzhou section of Jing-Hang Grand Canal in China. Environ. Sci. Pollut. Res. Int.. 19: 739-747.
66. Smith CJ, et al. 2005. T-Align, a Web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles. FEMS Microbiol. Ecol.. 54: 375-380.
67. Snelling W, et al. 2008. Colonization of broilers by Campylobacter jejuni internalized within Acanthamoeba castellanii. Arch. Microbiol.. 189: 175-179.
68. Snelling WJ, McKenna JP, Lecky DM, Dooley JS. 2005. Survival of Campylobacter jejuni in waterborne protozoa. Appl. Environ. Microbiol.. 71: 5560-5571.
69. Tauxe RV, Hargrett-Bean N, Patton CM, Wachsmuth IK. 1988. Campylobacter isolates in the United States, 1982-1986. MMWR CDC Surveill. Summ.. 37: 1-13.
70. Valster RM, Wullings BA, Bakker G, Smidt H, van der Kooij D. 2009. Free-living protozoa in two unchlorinated drinking water supplies, identified by phylogenic analysis of 18S rRNA gene sequences. Appl. Environ. Microbiol.. 75: 4736-4746.
71. Walsby AE, Holland DP. 2006. Sinking velocities of phytoplankton measured on a stable density gradient by laser scanning. J. R. Soc. Interface. 3: 429-439.
72. Williams R, et al. 2006. Amplification of complex gene libraries by emulsion PCR. Nat. Methods. 3: 545-550.
73. Zia S, et al. 2003. Health problems following Campylobacter jejuni enteritis in a Lancashire population. Rheumatology. 42: 1083-1088.