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

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 13 C-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 OPEN ACCESS Diversity 2013, 5 642 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.

Investigation into the fungal diversity within different regions of the gastrointestinal tract of <em>Panaque nigrolineatus</em>, a wood-eating fish

“…Our finding that P. nigrolineatus fed a wood-diet or a mixed-diet has different fungal communities is consistent with previous and current research showing similar variations for the bacterial communities in different regions of the GI tract [30, McDonald, Watts and Schreier, manuscript in preparation]. Of particular interest is the hindgut, which contains cellulolytic bacteria [29] , [30] , [31] as well as sequences similar to C. macrocephala , which has been associated with waterlogged wood [63] , [64] ; any relationship between these bacteria and fungi and their role in the fish GI tract remains to be determined.…”

“…Using 16S rRNA and culture-based analyses, the enteric bacterial community of P. nigrolineatus appears distinct and specialised in each region of the GI tract. The dominant bacteria have 16S rRNA gene sequences similar to Proteobacteria, Firmicutes, Bacteriodetes and Actinobacteria [30] , [31] , [32] . The midgut contains phylotypes with high sequence similarity to cellulose degrading bacteria Clostridium, Cellulomonas, Bacteroides, Eubacterium and Aeromonas spp.…”

“…that are capable of in situ nitrogen fixation [32] . The hindgut is dominated by Bacteroidetes [31] , [32] . Bacterial species richness has been shown to decrease distally from foregut, through to the midgut and hindgut.…”

Fish Gut Microbiome: Current Approaches and Future Perspectives

“…Li et al, showed that gut bacterial community of grass carp is dominated by cellulolytic Aeromonas, followed by Enterobacter, Enterococcus, Citrobacter, Bacillus, Raoultella, Klebsiella, Hydrotalea, Pseudomonas, Brevibacillus and that an increase in intake of plant-fibre increases the diversity of cellulolytic bacteria [36]. Cellulose degrading bacteria Clostridium, Aeromonas, Cellulomonas and Bacteroides along with other nitrogen fixing species are reported to provide assimilable carbon in the wood eating fish Panaque nigrolineatus [38,39]. Clostridia also dominate the gut microbial flora in different marine herbivorous fish species [40].…”

Impact of Phanerochaete chrysosporium on the Functional Diversity of Bacterial Communities Associated with Decaying Wood

“…While they are less studied, bacteria are also part of the decaying-wood microbial diversity [ 9 ] and are expected to contribute to wood decay. Indeed, tree species and wood decay class have been shown to significantly shape the structure of wood-inhabiting bacterial communities [ 10 ] and numerous bacteria present the capability of decomposing wood carbohydrates such as cellulose [ 11 – 12 ] and hemicelluloses [ 13 – 14 ]. Moreover, a few bacteria have also been described as being involved in lignin degradation [ 15 – 17 ].…”