Comparison of DNA extraction protocols for the analysis of gut microbiota in fishes

FEMS Microbiology Letters

Volumn 362, Issue 5, 2015, Pages

  Larsen, Andrea M ^a   Mohammed, Haitham H ^a   Arias, Covadonga R ^a  

^a AUBURN UNIVERSITY   (United States)

Author keywords

Fish gut; Microbial community; RISA

Indexed keywords

BACTERIAL DNA; RNA 16S;

ANALYTIC METHOD; ANIMAL FOOD; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA EXTRACTION; DNA FINGERPRINTING; FECES ANALYSIS; FISH; FREEZING; INTERMETHOD COMPARISON; INTESTINE EXAMINATION; INTESTINE FLORA; MICROBIAL COMMUNITY; NONHUMAN; PRIORITY JOURNAL; RIBOSOMAL INTERGENIC SPACER ANALYSIS; ANIMAL; COMPARATIVE STUDY; DNA SEQUENCE; FECES; GENETICS; INTESTINE; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; POLYMERASE CHAIN REACTION;

ANIMALS; DNA, BACTERIAL; FECES; FISHES; INTESTINES; MICROBIOTA; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84943249717     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1093/femsle/fnu031     Document Type: Article

References (75)

1. Abd El-Rhman AM, Khattab YAE, Shalaby AME. Micrococcus luteus and Pseudomonas species as probiotics for promoting the growth performance and health of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immun 2009;27:175-80.
2. Abid A, Davies SJ, Waines P, et al. Dietary synbiotic application modulates Atlantic salmon (Salmo salar) intestinal microbial communities and intestinal immunity. Fish Shellfish Immun 2013;35:1948-56.
3. Al-Harbi AH, Uddin N. Quantitative and qualitative studies on bacterial flora of hybrid tilapia (Oreochromis niloticus x Oaureus) cultured in earthen ponds in Saudi Arabia. Aquac Res 2003;34:43-8.
4. Arias CR, Abernathy JW, Liu Z. Combined use of 16S ribosomal DNA and automated ribosomal intergenic spacer analysis to study the bacterial community in catfish ponds. Lett Appl Microbiol 2006;43:287-92.
5. Ariefdjohan MW, Savaiano DA, Nakatsu CH. Comparison of DNA extraction kits for PCR-DGGE analysis of human intestinal microbial communities from fecal specimens. Nutr J 2010;9:23.
6. Bahl MI, Bergstrom A, Licht TR. Freezing fecal samples prior to DNA extraction affects the Firmicutes to Bacteroidetes ratio determined by downstream quantitative PCR analysis. FEMS Microbiol Lett 2012;329:193-7.
7. Barbosa MC, Jatoba A, Vieira FD, et al. Cultivation of juvenile fat snook (Centropomus parallelus Poey, 1860) fed probiotic in laboratory conditions. Braz Arch Biol Techn 2011;54:795-801.
8. Carda-Dieguez M, Mira A, Fouz B. Pyrosequencing survey of intestinal microbiota diversity in cultured sea bass (Dicentrarchus labrax) fed functional diets. FEMS Microbiol Ecol 2013;87:451-9.
9. Casamayor EO, Massana R, Benlloch S, et al. Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ Microbiol 2002;4:338-48.
10. Cipriano R. Far from superficial: microbial diversity associated with the dermal mucus of fish. In: Cipriano R, Schelkunov I (eds). Health and Diseases of Aquatic Organisms: Bilateral Perspectives. East Lansing, MI: MSU Press, 2011, 156-67.
11. Clarke KR, Gorley RN. PRIMER v6: User Manual/Tutorial. Plymouth, UK: Primer-E Ltd, 2006.
12. Clements KD, Pasch IBY, Moran D, et al. Clostridia dominate 16S rRNA gene libraries prepared from the hindgut of temperate marine herbivorous fishes. Mar Biol 2007;150:1431-40.
13. Delcroix J, Gatesoupe FJ, Desbruyeres E, et al. The effects of dietary marine protein hydrolysates on the development of sea bass larvae, Dicentrarchus labrax, and associated microbiota. Aquacult Nutr 2014; 21:98-104.
14. Dhanasiri AKS, Brunvold L, Brinchmann MF, et al. Changes in the intestinal microbiota of wild Atlantic cod Gadus morhua L. upon captive rearing. Microbial Ecol 2011;61:20-30.
15. Di Maiuta N, Schwarzentruber P, Schenker M, et al. Microbial population dynamics in the faeces of wood-eating loricariid catfishes. Lett Appl Microbiol 2013;56:401-7.
16. Din ARJM, Razak SA, Sabaratnam V. Effect of mushroom supplementation as a prebiotic compound in super worm based diet on growth performance of red tilapia fingerlings. Sains Malays 2012;41:1197-203.
17. Etzion A, Gillor O, Harpaz S, et al. Dietary supplementation of probiotic bacteria: effect on immune function and resistance to bacterial infection in barramundi, Lates calcarifer (Bloch, 1790). Isr J Aquacult-Bamid 2011;63:1-9.
18. Fisher MM, Triplett EW. Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microb 1999;65:4630-6.
19. Gatesoupe FJ, Huelvan C, Le Bayon N, et al. The effects of dietary carbohydrate sources and forms on metabolic response and intestinal microbiota in sea bass juveniles, Dicentrarchus labrax. Aquaculture 2014;422-423:47-53.
20. Ghosh S, Sinha A, Sahu C. Dietary probiotic supplementation in growth and health of live-bearing ornamental fishes. Aquacult Nutr 2008;14:289-99.
21. Grisez L, Reyniers J, Verdonck L, et al. Dominant intestinal microflora of sea bream and sea bass larvae, from two hatcheries, during larval development. Aquaculture 1997;155:387-99.
22. Griswold BL, Tubb RA. Food of yellow perch, white bass, freshwater drum, and channel catfish in Sandusky Bay, Lake Erie. Ohio J Sci 1977;77:43-7.
23. Harris NJ. Seasonal food habits of bluegills in Richmond Lake, South Dakota. Proc S D Acad Sci 1999;78:79-85.
24. Hartviksen M, Vecino JLG, Ringo E, et al. Alternative dietary protein sources for Atlantic salmon (Salmo salar L.) effect on intestinal microbiota, intestinal and liver histology and growth. Aquacult Nutr 2014;20:381-98.
25. He S,Wu Z, Liu Y, et al. Effects of dietary 60 g kg-1 dried distiller's grains in least-cost practical diets on production and gut allochthonous bacterial composition of cage-cultured fish: comparison among fish species with different natural food habits. Aquacult Nutr 2013;19:765-22.
26. Heikkinen J, Vielma J, Kemilainen O, et al. Effects of soybean meal based diet on growth performance, gut histopathology and intestinal microbiota of juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture 2006;261:259-68.
27. Hickley P, North R, Muchiri SM, et al. The diet of largemouth bass, Micropterus salmoides, in Lake Naivasha, Kenya. J Fish Biol 1994;44:607-19.
28. Hovda MB, Lunestad BT, Fontanillas R, et al. Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture 2007;272:581-8.
29. Jaafar RM, Kania PW, Larsen AH, et al. Gut microbiota changes in rainbow trout, Oncorhynchus mykiss (Walbaum), during organic acid feed supplementation and Yersinia ruckeri infection. J Fish Dis 2013;36:599-606.
30. Jatoba A, Vieira FD, Neto CB, et al. Lactic-acid bacteria isolated from the intestinal tract of Nile tilapia utilized as probiotic. Pesquisa Agropecu Bras 2008;43:1201-7.
31. Jearld A, Brown BE. Food of the channel catfish (Ictalurus punctatus) in a southern Great Plains reservoir. Am Midl Nat 1971;86:110-5.
32. Kim DH, Brunt J, Austin B. Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss). J Appl Microbiol 2007;102:1654-64.
33. KonstantinosAK, Meziti A, Mente E, et al. Dietary differences are reflected on the gut prokaryotic community structure of wild and commercially reared sea bream (Sparus aurata). MicrobiologyOpen 2014;3:718-28.
34. Kumar R, Mukherjee SC, Ranjan R, et al. Enhanced innate immune parameters in Labeo rohita (Ham.) following oral administration of Bacillus subtilis. Fish Shellfish Immun 2008;24:168-72.
35. Lantz PG, Matsson M, Wadstrom T, et al. Removal of PCR inhibitors from human faecal samples through the use of an aqueous two-phase system for sample preparation prior to PCR. J Microbiol Meth 1997;28:159-67.
36. Larsen A, Tao Z, Bullard SA, et al. Diversity of the skin microbiota of fishes: evidence for host species specificity. FEMS Microbiol Ecol 2013;85:483-94.
37. Larsen AM, Mohammed HH, Arias CR. Characterization of the gut microbiota of three commercially valuable warmwater fish species. J Appl Microbiol 2014;116:1396-404.
38. Li F, Hullar MAJ, Lampe JW. Optimization of terminal restriction fragment polymorphism (TRFLP) analysis of human gut microbiota. J Microbiol Meth 2007;68:303-11.
39. McOrist AL, Jackson M, Bird AR. A comparison of five methods for extraction of bacterial DNA from human faecal samples. J Microbiol Meth 2002;50:131-9.
40. Maukonen J, Simoes C, Saarela M. The currently used commercial DNA-extraction methods give different results of clostridial and actinobacterial populations derived from human fecal samples. FEMS Microbiol Ecol 2012;79:697-708.
41. Merrifield DL, Burnard D, Bradley G, et al. Microbial community diversity associated with the intestinal mucosa of farmed rainbow trout (Oncoryhnchus mykiss Walbaum). Aquac Res 2009;40:1064-72.
42. Molbak L, Sommer HM, Johnsen K, et al. Freezing at -80°C distorts the DNA composition of bacterial communities in intestinal samples. Curr Issues Intest Microbiol 2006;7:29-34.
43. Monteiro L, Bonnemaison D, Vekris A, et al. Complex polysaccharides as PCR inhibitors in feces: Helicobacter pylori model. J Clin Microbiol 1997;35:995-8.
44. Monteiro L, Gras N, Vidal R, et al. Detection of Helicobacter pylori DNA in human feces by PCR: DNA stability and removal of inhibitors. J Microbiol Meth 2001;45:89-94.
45. Mouchet MA, Bouvier C, Bouvier T, et al. Genetic difference but functional similarity among fish gut bacterial communities throughmolecular and biochemical fingerprints. FEMS Microbiol Ecol 2012;79:568-80.
46. Najdegerami EH, Tran TN, Defoirdt T, et al. Effects of poly-sshydroxybutyrate (PHB) on Siberian sturgeon (Acipenser baerii) fingerlings performance and its gastrointestinal tract microbial community. FEMS Microbiol Ecol 2012;79:25-33.
47. Nayak SK. Role of gastrointestinal microbiota in fish. Aquac Res 2010;41:1553-73.
48. Nelson EA, Palombo EA, Knowles SR. Comparison of methods for the extraction of bacterial DNA from human faecal samples for analysis by real-time PCR. In: Mendez-Vilas A, (ed). Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, Vol. 2. Badajoz, Spain: Formatex Research Center, 2010, 1479-85.
49. Nelson JA,Wubah DA, Whitmer ME, et al.Wood-eating catfishes of the genus Panaque: gut microflora and cellulolytic enzyme activities. J Fish Biol 1999;54:1069-82.
50. Ni J, Yan Q, Zhang T. Factors influencing the grass carp gut microbiome and its effect on metabolism. FEMS Microbiol Ecol 2013;87:704-14.
51. OlsonMH, Young BP. Patterns of diet and growth in co-occurring populations of largemouth bass and smallmouth bass. T Am Fish Soc 2003;132:1207-13.
52. Pesaro M, Widmer F, Nicollier G, et al. Effects of freeze-thaw stress during soil storage onmicrobial communities and methidathion degradation. Soil Biol Biochem 2003;35:1049-61.
53. Qiagen. DNeasy Blood & Tissue Handbook. Valencia, CA, 2006.
54. Qiagen. QIAamp DNA Stool Handbook. Valencia, CA, 2010.
55. RamosMA,Weber B, Goncalves JF, et al. Dietary probiotic supplementation modulated gut microbiota and improved growth of juvenile rainbowtrout (Oncorhynchusmykiss). Comp Biochem Phys A 2013;166:302-7.
56. Ranjard L, Lejon DPH, Mougel C, et al. Sampling strategy in molecularmicrobial ecology: influence of soil sample size on DNA fingerprinting analysis of fungal and bacterial communities. Environ Microbiol 2003;5:1111-20.
57. Rawls JF, Mahowald MA, Ley RE, et al. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 2006;127:423-33.
58. Ringo E, Olsen RE. The effect of diet on aerobic bacterial flora associated with intestine of Arctic charr (Salvelinus alpinus L.). J Appl Microbiol 1999;86:22-8.
59. Ringo E, Sperstad S, Myklebust R, et al. Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.)-the effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture 2006;261: 829-41.
60. Rissanen AJ, Kurhela E, Aho T, et al. Storage of environmental samples for guaranteeing nucleic acid yields for molecular microbiological studies. Appl Microbiol Biot 2010;88: 977-84.
61. Sakata T, Okabayashi J, Kakimoto D. Variations in the intestinal microflora of tilapia reared in fresh and sea water. B Jpn Soc Sci Fish 1980;46:313-7.
62. Salonen A, Nikkila J, Jalanka-Tuovinen J, et al. Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J Microbiol Meth 2010;81:127-34.
63. Seaburg KG, Moyle JB. Feeding habits, digestive rates, and growth of some Minnesota warmwater fishes. T Am Fish Soc 1964;93:269-85.
64. Silva FC, Nicoli JR, Zambonino-Infante JL, et al. Influence of the diet on the microbial diversity of faecal and gastrointestinal contents in gilthead sea bream (Sparus aurata) and intestinal contents in goldfish (Carassius auratus). FEMS Microbiol Ecol 2011;78:285-96.
65. Skrodenyte-Arbaciauskiene V, Sruoga A, Butkauskas D, et al. Phylogenetic analysis of intestinal bacteria of freshwater salmon Salmo salar and sea trout Salmo trutta trutta and diet. Fisheries Sci 2008;74:1307-14.
66. Smriga S, Sandin SA, Azam F. Abundance, diversity, and activity of microbial assemblages associated with coral reef fish guts and feces. FEMS Microbiol Ecol 2010;73:31-42.
67. Spanggaard B, Huber I, Nielsen J, et al. The microflora of rainbow trout intestine: a comparison of traditional and molecular identification. Aquaculture 2000;182:1-5.
68. Tanu, Deobagkar DD, Khandeparker R, et al. A study on bacteria associated with the intestinal tract of farmed yellow seahorse, Hippocampus kuda (Bleeker, 1852): characterization and extracellular enzymes. Aquac Res 2012;43:386-94.
69. Turner WR. Food habits of the bluegill Lepomis macrochirus macrochirus (Rafinesque), in eighteen Kentucky farm ponds during April and May. T Kentucky Acad Sci 1955;16:98-101.
70. Uchii K, Matsui K, Yonekura R, et al. Genetic and physiological characterization of the intestinal bacterial microbiota of bluegill (Lepomis macrochirus) with three different feeding habits. Microbial Ecol 2006;51:277-84.
71. Wheeler AP, Allen MS. Habitat and diet partitioning between shoal bass and largemouth bass in the Chipola River, Florida. T Am Fish Soc 2003;132:438-49.
72. Wilson IG. Inhibition and facilitation of nucleic acid amplification. Appl Environ Microb 1997;63:3741-51.
73. Wu GD, Lewis JD, Hoffmann C, et al. Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiol 2010;10:206.
74. Yu Z, Mohn WW. Bacterial diversity and community structure in an aerated lagoon revealed by ribosomal intergenic spacer analysis and 16S ribosomal DNA sequencing. Appl EnvironMicrob 2001;67:1565-74.
75. Zoetendal EG, Ben-Amor K, Akkermans ADL, et al. DNA isolation protocols affect the detection limit of PCR approaches of bacteria in samples from the human gastrointestinal tract. Syst Appl Microbiol 2001;24:405-10.