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Diversity  2013 

Examination of a Culturable Microbial Population from the Gastrointestinal Tract of the Wood-Eating Loricariid Catfish Panaque nigrolineatus

DOI: 10.3390/d5030641

Keywords: microbial diversity, cellulose degradation, enrichment, Panaque, gastrointestinal tract

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Abstract:

Fish play a critical role in nutrient cycling and organic matter flow in aquatic environments. However, little is known about the microbial diversity within the gastrointestinal tracts that may be essential in these degradation activities. Panaque nigrolineatus is a loricariid catfish found in the Neotropics that have a rare dietary strategy of consuming large amounts of woody material in its natural environment. As a consequence, the gastrointestinal (GI) tract of P. nigrolineatus is continually exposed to high levels of cellulose and other recalcitrant wood compounds and is, therefore, an attractive, uncharacterized system to study microbial community diversity. Our previous 16S rRNA gene surveys demonstrated that the GI tract microbial community includes phylotypes having the capacity to degrade cellulose and fix molecular nitrogen. In the present study we verify the presence of a resident microbial community by fluorescence microscopy and focus on the cellulose-degrading members by culture-based and 13C-labeled cellulose DNA stable-isotope probing (SIP) approaches. Analysis of GI tract communities generated from anaerobic microcrystalline cellulose enrichment cultures by 16S rRNA gene analysis revealed phylotypes sharing high sequence similarity to known cellulolytic bacteria including Clostridium, Cellulomonas, Bacteroides, Eubacterium and Aeromonas spp. Related bacteria were identified in the SIP community, which also included nitrogen-fixing Azospirillum spp. Our ability to enrich for specialized cellulose-degrading communities suggests that the P. nigrolineatus GI tract provides a favorable environment for this activity and these communities may be involved in providing assimilable carbon under challenging dietary conditions.

References

[1]  Power, M.E. Effects of fish in river food webs. Science 1990, 250, 811–814.
[2]  Schindler, D.E.; Carpenter, S.R.; Cole, J.J.; Kitchell, J.F.; Pace, M.L. Influence of food web structure on carbon exchange between lakes and the atmosphere. Science 1997, 277, 248–251, doi:10.1126/science.277.5323.248.
[3]  Vanni, M.J. Nutrient cycling by animals in freshwater ecosystems. Annu. Rev. Ecol. Syst. 2002, 33, 341–370, doi:10.1146/annurev.ecolsys.33.010802.150519.
[4]  Taylor, B.W.; Flecker, A.S.; Hall, R.O. Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 2006, 313, 833–836, doi:10.1126/science.1128223.
[5]  McIntyre, P.B.; Jones, L.E.; Flecker, A.S.; Vanni, M.J. Fish extinctions alter nutrient recycling in tropical freshwaters. Proc. Natl. Acad. Sci. USA 2007, 104, 4461–4466, doi:10.1073/pnas.0608148104.
[6]  Rawls, J.F.; Mahowald, M.A.; Ley, R.E.; Gordon, J.I. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 2006, 127, 423–433, doi:10.1016/j.cell.2006.08.043.
[7]  Sullam, K.E.; Essinger, S.D.; Lozupone, C.A.; O’Connor, M.P.; Rosen, G.L.; Knight, R.O.; Kilham, S.S.; Russell, J.A. Environmental and ecological factors that shape the gut bacterial communities of fish: A meta-analysis. Mol. Ecol. 2012, 21, 3363–3378, doi:10.1111/j.1365-294X.2012.05552.x.
[8]  Rawls, J.F.; Samuel, B.S.; Gordon, J.I. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. USA 2004, 101, 4596–4601, doi:10.1073/pnas.0400706101.
[9]  Bates, J.M.; Mittge, E.; Kuhlman, J.; Baden, K.N.; Cheesman, S.E.; Guillemin, K. Distinct signals fromthe microbiota promote different aspects of zebrafish gut differentiation. Dev. Biol. 2006, 297, 374–386, doi:10.1016/j.ydbio.2006.05.006.
[10]  Sugita, H.; Miyajima, C.; Deguchi, Y. Vitamin B12 producing ability of the intestinal microfora of fresh-water fish. Aquaculture 1991, 92, 267–276, doi:10.1016/0044-8486(91)90028-6.
[11]  Sekirov, I.; Finlay, B.B. The role of the intestinal microbiota in enteric infection. J. Physiol. 2009, 587, 4159–4167, doi:10.1113/jphysiol.2009.172742.
[12]  Choat, J.H.; Clements, K.D. Vertebrate herbivores in marine and terrestrial environments: A nutritional ecology perspective. Annu. Rev. Ecol. Syst. 1998, 29, 375–403, doi:10.1146/annurev.ecolsys.29.1.375.
[13]  Choat, J.H.; Clements, K.D.; Robbins, W.D. The trophic status of herbivorous fishes on coral reefs 1: Dietary analyses. Mar. Biol. 2002, 140, 613–623, doi:10.1007/s00227-001-0715-3.
[14]  Choat, J.H.; Robbins, W.D.; Clements, K.D. The trophic status of herbivorous fishes on coral reefs II: Food processing modes and trophodynamics. Mar. Biol. 2004, 145, 445–454.
[15]  Armbruster, J.W. Phylogenetic relationships of the suckermouth armoured catfishes (Loricariidae) with emphasis on the Hypostominae and the Ancistrinae. Zool. J. Linn. Soc. 2004, 141, 1–80, doi:10.1111/j.1096-3642.2004.00109.x.
[16]  Lujan, N.K.; Winemiller, K.O.; Armbruster, J.W. Trophic diversity in the evolution and community assembly of loricariid catfishes. BMC Evol. Biol. 2012, 26, 124–136.
[17]  Saul, W.G. An ecological study of fishes at a site in upper amazonian ecuador. Proc. Acad. Nat. Sci. USA 1975, 127, 93–114.
[18]  Delariva, R.L.; Agostinho, A.A. Relationship between morphology and diets of six neotropical loricariids. J. Fish Biol. 2001, 58, 832–847, doi:10.1111/j.1095-8649.2001.tb00534.x.
[19]  Salvador, L.F., Jr.; Salvador, G.N.; Santos, G.B. Morphology of the digestive tract and feeding habits of Loricaria lentiginosa Isbrücker, 1979 in a Brazilian reservoir. Acta Zool. 2009, 90, 101–109, doi:10.1111/j.1463-6395.2008.00336.x.
[20]  Schaefer, S.A.; Stewart, D.J. Systematics of Panaque dentex species group (Siluriformes, Loricariidae) wood-eating armored catfishes from tropical South America. Ichthyol. Explor. Freshw. 1993, 4, 309–342.
[21]  Armbruster, J.W. The Species of the Hypostomus Cochliodon Group (Siluriformes: Loricariidae). Zootaxa 2003, 249, 1–60.
[22]  Geerinckx, T.; de Poorter, J.; Adriaens, D. Morphology and development of teeth and epidermal brushes in loricariid catfishes. J. Morphol. 2007, 268, 805–814, doi:10.1002/jmor.10547.
[23]  Lujan, N.K.; Armbruster, J.W. Morphological and functional diversity of the mandible in suckermouth armored catfishes (Siluriformes: Loricariidae). J. Morphol. 2012, 273, 24–39, doi:10.1002/jmor.11003.
[24]  Nonogaki, H.; Nelson, J.A.; Patterson, W.P. Dietary histories of herbivorous loricariid catfishes: evidence from δ13C values of otoliths. Environ. Biol. Fishes 2007, 78, 13–21, doi:10.1007/s10641-006-9074-8.
[25]  German, D. Inside the guts of wood-eating catfishes: Can they digest wood? J. Comp. Physiol. B 2009, 179, 1011–1023, doi:10.1007/s00360-009-0381-1.
[26]  Clements, K.D.; Gleeson, V.P.; Slaytor, M. Short-chain fatty acid metabolism in temperate marine herbivorous fish. J. Comp. Physiol. B 1994, 164, 372–377, doi:10.1007/BF00302552.
[27]  German, D.; Bittong, R. Digestive enzyme activities and gastrointestinal fermentation in wood-eating catfishes. J. Comp. Physiol. B 2009, 179, 1025–1042, doi:10.1007/s00360-009-0383-z.
[28]  Lujan, N.K.; German, D.P.; Winemiller, K.O. Do wood-grazing fishes partition their niche?: morphological and isotopic evidence for trophic segregation in Neotropical Loricariidae. Funct. Ecol. 2011, 28, 1327–1338.
[29]  Lynd, L.R.; Weimer, P.J.; van Zyl, W.H.; Pretorius, I.S. Microbial cellulose utilization: Fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 2002, 66, 506–577, doi:10.1128/MMBR.66.3.506-577.2002.
[30]  Mouchet, M.A.; Bouvier, C.; Bouvier, T.; Troussellier, M.; Escalas, A.; Mouillot, D. Genetic difference but functional similarity among fish gut bacterial communities through molecular and biochemical fingerprints. FEMS Microbiol. Ecol. 2012, 79, 568–580, doi:10.1111/j.1574-6941.2011.01241.x.
[31]  Leschine, S.B. Cellulose degradation in anaerobic environments. Ann. Rev. Microbiol. 1995, 8, 237–299.
[32]  Wilson, D.B. Microbial diversity of cellulose hydrolysis. Curr. Opin. Microbiol. 2011, 14, 259–263.
[33]  Breznak, J.A.; Brune, A. Role of microorganisms in the digestion of lignocellulose by termites. Annu. Rev. Entomol. 1994, 39, 453–487, doi:10.1146/annurev.en.39.010194.002321.
[34]  Cleveland, L.R. Symbiosis between termites and their intestinal protozoa. Proc. Natl. Acad. Sci. USA 1923, 9, 424–428, doi:10.1073/pnas.9.12.424.
[35]  Distel, D.L.; Beaudoin, D.J.; Morrill, W. Coexistence of multiple proteobacterial endosymbionts in the gills of the wood-boring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). Appl. Environ. Microbiol. 2002, 68, 6292–6299, doi:10.1128/AEM.68.12.6292-6299.2002.
[36]  Pellens, R.; Grandcolas, P.; da Silva Neto, I.D. A new and independently evolved case of xylophagy and the presence of intestinal flagellates in the cockroach Parasphaeria boleiriana (Dictyoptera, Blaberidae, Zetoborinae) from the remnants of the Brazilian Atlantic forest. Can. J. Zool. 2002, 80, 350–360, doi:10.1139/z01-230.
[37]  Waterbury, J.B.; Turner, R.D.; Calloway, C.B. A cellulolytic nitrogen-fixing bacterium cultured from the gland of Deshayes in shipworms (Bivalvia: Teredinidae). Science 1983, 221, 1401–1403.
[38]  Bayer, E.A.; Chanzy, H.; Lamed, R.; Shoham, Y. Cellulose, cellulases and cellulosomes. Curr. Opin. Struct. Biol. 1998, 8, 548–557, doi:10.1016/S0959-440X(98)80143-7.
[39]  Talbot, J.M.; Treseder, K.K. Interactions among lignin, cellulose, and nitrogen drive litter chemistry–decay relationship. Ecology 2011, 93, 345–354, doi:10.1890/11-0843.1.
[40]  Zaldivar, J.; Nielsen, J.; Olsson, L. Ethanol fuel production from lignocellulose: A challenge for metabolic engineering and process integration. Appl. Microbiol. Biotechnol. 2001, 56, 17–34, doi:10.1007/s002530100624.
[41]  Ragauskas, A.J.; Williams, C.K.; Davison, B.H.; Britovsek, G.; Cairney, J.; Eckert, C.A.; Frederick, W.J.; Hallett, J.P.; Leak, D.J.; Liotta, C.L.; et al. The path forward for biofuels and biomaterials. Science 2006, 311, 484–489, doi:10.1126/science.1114736.
[42]  McDonald, R.; Schreier, H.J.; Watts, J.E.M. Phylogenetic Analysis of Microbial Communities in different regions of the gastrointestinal tract in Panaque nigrolineatus, a wood-eating fish. PLoS One 2012, 7, e48018, doi:10.1371/journal.pone.0048018.
[43]  Sowers, K.R.; Noll, K.M. Techniques for Anaerobic Growth. In Archaea: A Laboratory Manual; Robb, F.T., Sowers, K.R., DasSharma, S., Place, A.R., Schreier, H.J., Fleischmann, E.M., Eds.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 1995; pp. 15–48.
[44]  Lane, D.J. 16S/23S rRNA Sequencing. In Nucleic Acid Techniques in Bacterial Systematics; Stackebrandt, E., Ed.; John Wiley and Sons Ltd.: Cambridge, UK, 1991; pp. 115–175.
[45]  Ferris, M.J.; Muyzer, G.; Ward, D.M. Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl. Environ. Microbiol. 1996, 62, 340–346.
[46]  Warshaw, J.E.; Leschine, S.B.; Canale-Parola, E. Anaerobic cellulolytic bacteria from wetwood of living trees. Appl. Environ. Microbiol. 1985, 50, 807–811.
[47]  Neufeld, J.D.; Vohra, J.; Dumont, M.G.; Lueders, T.; Manefield, M.; Friedrich, M.W.; Murrell, J.C. DNA stable-isotope probing. Nat. Protocols 2007, 2, 860–866, doi:10.1038/nprot.2007.109.
[48]  Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403–410.
[49]  Swidsinski, A.; Weber, J.; Loening-Baucke, V.; Hale, L.P.; Lochs, H. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J. Clin. Microbiol. 2005, 43, 3380–3389, doi:10.1128/JCM.43.7.3380-3389.2005.
[50]  Rogers, G.M.; Baecker, A.A.W. Clostridium xylanolyticum sp. nov., an anaerobic xylanolytic bacterium from decayed Pinus patula wood chips. Int. J. Syst. Bacteriol. 1991, 41, 140–143.
[51]  Jeong, H.; Lim, Y.W.; Yi, H.; Sekiguchi, Y.; Kamagata, Y.; Chun, J. Anaerosporobacter mobilis gen. nov., sp. nov., isolated from forest soil. Int. J. Syst. Evol. Microbiol. 2007, 57, 1784–1787.
[52]  Manter, D.; Hunter, W.; Vivanco, J. Enterobacter soli sp. nov.: A lignin-degrading γ-Proteobacteria isolated from soil. Curr. Microbiol. 2011, 62, 1044–1049.
[53]  Yoon, M.-H.; Ten, L.N.; Im, W.-T.; Lee, S.-T. Cellulomonas chitinilytica sp. nov., a chitinolytic bacterium isolated from cattle-farm compost. Int. J. Syst. Evol. Microbiol. 2008, 58, 1878–1884.
[54]  Kim, C.H. Characterization and substrate specificity of an endo-beta-1,4-D-glucanase I (Avicelase I) from an extracellular multienzyme complex of Bacillus circulans. Appl. Environ. Microbiol. 1995, 61, 959–965.
[55]  Singh, B.; Bhat, T.K.; Sharma, O.P.; Kanwar, S.S.; Rahi, P.; Gulati, A. Isolation of tannase-producing Enterobacter ludwigii GRT-1 from the rumen of migratory goats. Small Rumin. Res. 2012, 102, 172–176, doi:10.1016/j.smallrumres.2011.06.013.
[56]  Buchman, A.L.; Pickett, M.J.; Mann, L.; Ament, M.E. Central venous catheter infection caused by Moraxella osloensis in a patient receiving home parenteral nutrition. Diagn. Microbiol. Infect. Dis. 1993, 17, 163–166, doi:10.1016/0732-8893(93)90028-6.
[57]  Debelian, G.J.; Olsen, I.; Tronstad, L. Profiling of Propionibacterium acnes recovered from root canal and blood during and after endodontic treatment. Endod. Dent. Traumatol. 1992, 8, 248–254, doi:10.1111/j.1600-9657.1992.tb00253.x.
[58]  Figueira, V.; Vaz-Moreira, I.; Silva, M.; Manaia, C.M. Diversity and antibiotic resistance of Aeromonas spp. in drinking and waste water treatment plants. Water Res. 2011, 45, 5599–5611, doi:10.1016/j.watres.2011.08.021.
[59]  Wang, X.; Feng, Y.; Wang, H.; Qu, Y.; Yu, Y.; Ren, N.; Li, N.; Wang, E.; Lee, H.; Logan, B.E. Bioaugmentation for electricity generation from corn stover biomass using microbial fuel cells. Environ. Sci. Technol. 2009, 43, 6088–6093, doi:10.1021/es900391b.
[60]  Lednická, D.; Mergaert, J.; Cnockaert, M.C.; Swings, J. Isolation and identification of cellulolytic bacteria involved in the degradation of natural cellulosic fibres. Syst. Appl. Microbiol. 2000, 23, 292–299, doi:10.1016/S0723-2020(00)80017-X.
[61]  Halsall, D.M.; Gibson, A.H. Comparison of two cellulomonas strains and their interaction with azospirillum brasilense in degradation of wheat straw and associated nitrogen fixation. Appl. Environ. Microbiol. 1986, 51, 855–861.
[62]  G??ner, A.S.; Küsel, K.; Schulz, D.; Trenz, S.; Acker, G.; Lovell, C.R.; Drake, H.L. Trophic interaction of the aerotolerant anaerobe Clostridium intestinale and the acetogen Sporomusa rhizae sp. nov. isolated from roots of the black needlerush Juncus roemerianus. Microbiology 2006, 152, 1209–1219, doi:10.1099/mic.0.28725-0.
[63]  Chen, Y.; Vohra, J.; Murrell, J.C. Applications of DNA-Stable Isotope Probing in Bioremediation Studies. In Bioremediation, Methods in Molecular Biology; Cummings, S.P., Ed.; Humana Press: New York, NY, USA, 2010; pp. 129–138.
[64]  Leadbetter, J.R. Cultivation of recalcitrant microbes: Cells are alive, well and revealing their secrets in the 21st century laboratory. Curr. Opin. Microbiol. 2003, 6, 274–281, doi:10.1016/S1369-5274(03)00041-9.
[65]  Doolittle, W.F. Phylogenetic classification and the universal tree. Science 1999, 284, 2124–2128, doi:10.1126/science.284.5423.2124.
[66]  Roeselers, G.; Mittge, E.K.; Stephens, W.Z.; Parichy, D.M.; Cavanaugh, C.M.; Guillemin, K.; Rawls, J.F. Evidence for a core gut microbiota in the zebrafish. ISME J. 2011, 5, 1595–1608, doi:10.1038/ismej.2011.38.

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