Dataset Information

Pyrosequencing reveals high-temperature cellulolytic microbial consortia in Great Boiling Spring after in situ lignocellulose enrichment.

ABSTRACT: To characterize high-temperature cellulolytic microbial communities, two lignocellulosic substrates, ammonia fiber-explosion-treated corn stover and aspen shavings, were incubated at average temperatures of 77 and 85°C in the sediment and water column of Great Boiling Spring, Nevada. Comparison of 109,941 quality-filtered 16S rRNA gene pyrosequences (pyrotags) from eight enrichments to 37,057 quality-filtered pyrotags from corresponding natural samples revealed distinct enriched communities dominated by phylotypes related to cellulolytic and hemicellulolytic Thermotoga and Dictyoglomus, cellulolytic and sugar-fermenting Desulfurococcales, and sugar-fermenting and hydrogenotrophic Archaeoglobales. Minor enriched populations included close relatives of hydrogenotrophic Thermodesulfobacteria, the candidate bacterial phylum OP9, and candidate archaeal groups C2 and DHVE3. Enrichment temperature was the major factor influencing community composition, with a negative correlation between temperature and richness, followed by lignocellulosic substrate composition. This study establishes the importance of these groups in the natural degradation of lignocellulose at high temperatures and suggests that a substantial portion of the diversity of thermophiles contributing to consortial cellulolysis may be contained within lineages that have representatives in pure culture.

SUBMITTER: Peacock JP

PROVIDER: S-EPMC3612082 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Pyrosequencing reveals high-temperature cellulolytic microbial consortia in Great Boiling Spring after in situ lignocellulose enrichment.

Peacock Joseph P JP Cole Jessica K JK Murugapiran Senthil K SK Dodsworth Jeremy A JA Fisher Jenny C JC Moser Duane P DP Hedlund Brian P BP

PloS one 20130329 3

To characterize high-temperature cellulolytic microbial communities, two lignocellulosic substrates, ammonia fiber-explosion-treated corn stover and aspen shavings, were incubated at average temperatures of 77 and 85°C in the sediment and water column of Great Boiling Spring, Nevada. Comparison of 109,941 quality-filtered 16S rRNA gene pyrosequences (pyrotags) from eight enrichments to 37,057 quality-filtered pyrotags from corresponding natural samples revealed distinct enriched communities domi ...[more]

PMID: 23555835

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Project description:The complexity of microbial communities hinders our understanding of how microbial diversity and microbe-microbe interactions impact community functions. Here, using six independent communities originating from the refuse dumps of leaf-cutter ants and enriched using the plant polymer cellulose as the sole source of carbon, we examine how changes in bacterial diversity and interactions impact plant biomass decomposition. Over up to 60 serial transfers (∼8 months) using Whatman cellulose filter paper, cellulolytic ability increased and then stabilized in four enrichment lines and was variable in two lines. Bacterial community characterization using 16S rRNA gene amplicon sequencing showed community succession differed between the highly cellulolytic enrichment lines and those that had slower and more variable cellulose degradation rates. Metagenomic and metatranscriptomic analyses revealed that Cellvibrio and/or Cellulomonas dominated each enrichment line and produced the majority of cellulase enzymes, while diverse taxa were retained within these communities over the duration of transfers. Interestingly, the less cellulolytic communities had a higher diversity of organisms competing for the cellulose breakdown product cellobiose, suggesting that cheating slowed cellulose degradation. In addition, we found competitive exclusion as an important factor shaping all of the communities, with a negative correlation of Cellvibrio and Cellulomonas abundance within individual enrichment lines and the expression of genes associated with the production of secondary metabolites, toxins, and other antagonistic compounds. Our results provide insights into how microbial diversity and competition affect the stability and function of cellulose-degrading communities. IMPORTANCE Microbial communities are a key driver of the carbon cycle through the breakdown of complex polysaccharides in diverse environments including soil, marine systems, and the mammalian gut. However, due to the complexity of these communities, the species-species interactions that impact community structure and ultimately shape the rate of decomposition are difficult to define. Here, we performed serial enrichment on cellulose using communities inoculated from leaf-cutter ant refuse dumps, a cellulose-rich environment. By concurrently tracking cellulolytic ability and community composition and through metagenomic and metatranscriptomic sequencing, we analyzed the ecological dynamics of the enrichment lines. Our data suggest that antagonism is prevalent in these communities and that competition for soluble sugars may slow degradation and lead to community instability. Together, these results help reveal the relationships between competition and polysaccharide decomposition, with implications in diverse areas ranging from microbial community ecology to cellulosic biofuels production.

Project description:Enriched microbial communities, obtained from environmental samples through selective processes, can effectively contribute to lignocellulose degradation. Unfortunately, fully controlled industrial degradation processes are difficult to reach given the intrinsically dynamic nature and complexity of the microbial communities, composed of a large number of culturable and unculturable species. The use of less complex but equally effective microbial consortia could improve their applications by allowing for more controlled industrial processes. Here, we combined ecological theory and enrichment principles to develop an effective lignocellulose-degrading minimal active microbial Consortia (MAMC). Following an enrichment of soil bacteria capable of degrading lignocellulose material from sugarcane origin, we applied a reductive-screening approach based on molecular phenotyping, identification, and metabolic characterization to obtain a selection of 18 lignocellulose-degrading strains representing four metabolic functional groups. We then generated 65 compositional replicates of MAMC containing five species each, which vary in the number of functional groups, metabolic potential, and degradation capacity. The characterization of the MAMC according to their degradation capacities and functional diversity measurements revealed that functional diversity positively correlated with the degradation of the most complex lignocellulosic fraction (lignin), indicating the importance of metabolic complementarity, whereas cellulose and hemicellulose degradation were either negatively or not affected by functional diversity. The screening method described here successfully led to the selection of effective MAMC, whose degradation potential reached up 96.5% of the degradation rates when all 18 species were present. A total of seven assembled synthetic communities were identified as the most effective MAMC. A consortium containing Stenotrophomonas maltophilia, Paenibacillus sp., Microbacterium sp., Chryseobacterium taiwanense, and Brevundimonas sp. was found to be the most effective degrading synthetic community.

Project description:Despite multiple research efforts, the current strategies for exploitation of lignocellulosic plant matter are still far from optimal, being hampered mostly by the difficulty of degrading the recalcitrant parts. An interesting approach is to use lignocellulose-degrading microbial communities by using different environmental sources of microbial inocula. However, it remains unclear whether the inoculum source matters for the degradation process. Here, we addressed this question by verifying the lignocellulose degradation potential of wheat (Triticum aestivum) straw by microbial consortia generated from three different microbial inoculum sources, i.e., forest soil, canal sediment and decaying wood. We selected these consortia through ten sequential-batch enrichments by dilution-to-stimulation using wheat straw as the sole carbon source. We monitored the changes in microbial composition and abundance, as well as their associated degradation capacity and enzymatic activities. Overall, the microbial consortia developed well on the substrate, with progressively-decreasing net average generation times. Each final consortium encompassed bacterial/fungal communities that were distinct in composition but functionally similar, as they all revealed high substrate degradation activities. However, we did find significant differences in the metabolic diversities per consortium: in wood-derived consortia cellobiohydrolases prevailed, in soil-derived ones β-glucosidases, and in sediment-derived ones several activities. Isolates recovered from the consortia showed considerable metabolic diversities across the consortia. This confirmed that, although the overall lignocellulose degradation was similar, each consortium had a unique enzyme activity pattern. Clearly, inoculum source was the key determinant of the composition of the final microbial degrader consortia, yet with varying enzyme activities. Hence, in accord with Beyerinck's, "everything is everywhere, the environment selects" the source determines consortium composition.

Dataset Information

Pyrosequencing reveals high-temperature cellulolytic microbial consortia in Great Boiling Spring after in situ lignocellulose enrichment.

Publications

Pyrosequencing reveals high-temperature cellulolytic microbial consortia in Great Boiling Spring after in situ lignocellulose enrichment.

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