Defining the functional traits that drive bacterial decomposer community productivity

Evans, Rachael A.; Alessi, Anna; Bird, Susannah; McQueen‐Mason, Simon J.; Bruce, Neil C.; Brockhurst, Michael A.

doi:10.1038/ismej.2017.22

Cited by 35 publications

(42 citation statements)

References 38 publications

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“…The cellobiose-metabolizing, noncellulolytic microbes can be thought of as 'cheaters'; they used the cellobiose public goods without producing or secreting cellulases, reducing cellobiose availability for the cellulolytic microbes. Previous studies have also found that cheaters use public goods during cellulose degradation and during the breakdown of other polysaccharides (21,(47)(48)(49), and cheaters have been shown to have both detrimental and positive effects on the rate of degradation (25,50,51). Our data suggest that in enrichment lines 1A and 1B, degradation was slowed by high levels of β-glucosidase genes from diverse microbes (Fig.…”

Section: Signatures Of Competition Dominate In Enriched Communities supporting

confidence: 71%

Long-term cellulose enrichment selects for highly cellulolytic consortia and competition for public goods

Lewin

Davis

McDonald

et al. 2020

Preprint

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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), cellulolytic ability increased 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 and variably cellulolytic enrichment lines. 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 the communities, with the mutual exclusion of specific cellulolytic taxa within individual enrichment lines and the high expression of genes associated with the production of antagonistic compounds. Our results provide insights into how microbial diversity and competition affect the stability and function of cellulose-degrading communities.ImportanceMicrobial 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.

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Section: Signatures Of Competition Dominate In Enriched Communities supporting

confidence: 71%

Long-term cellulose enrichment selects for highly cellulolytic consortia and competition for public goods

Lewin

Davis

McDonald

et al. 2020

Preprint

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“…Biological richness (e.g. the number of functionally different genotypes within a community) is one factor that may be important (Bell et al, 2005;Duffy, 2009;Cardinale, 2011;Gravel et al, 2011;Peter et al, 2011;Bouvier et al, 2012;Cardinale et al, 2012;Dell'Anno et al, 2012;Hernandez-Raquet et al, 2013;Philippot et al, 2013;Johnson et al, 2015a;Evans et al, 2017;Stadler et al, 2017). Communities with higher biological richness are more likely to contain genotypes that have direct or indirect positive effects on the rate of a particular metabolic process (Loreau et al, 2001;Balvanera et al, 2006;Cardinale et al, 2006;Cardinale, 2011;Cardinale et al, 2012;Tilman et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…While positive associations between biological richness and the rates of particular metabolic processes have been observed (Bell et al, 2005;Cardinale, 2011;Gravel et al, 2011;Peter et al, 2011;Bouvier et al, 2012;Cardinale et al, 2012;Dell'Anno et al, 2012;Hernandez-Raquet et al, 2013;Philippot et al, 2013;Johnson et al, 2015a;Evans et al, 2017;Stadler et al, 2017), it remains unclear whether these positive associations are a general feature of the metabolic processes performed by microbial communities. For example, while many studies have observed positive associations between biological richness and the rates of some metabolic processes (Bell et al, 2005;Cardinale, 2011;Gravel et al, 2011;Peter et al, 2011;Bouvier et al, 2012;Cardinale et al, 2012;Dell'Anno et al, 2012;Hernandez-Raquet et al, 2013;Philippot et al, 2013;Johnson et al, 2015a;Evans et al, 2017;Stadler et al, 2017), other studies have not (Salonius, 1981;Griffiths et al, 2001;Wertz et al, 2006;Szabó et al, 2007;Peter et al, 2011;Pholchan et al, 2013;Graham et al, 2014;Roger et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Generality of associations between biological richness and the rates of metabolic processes across microbial communities

Patsch

Vliet

Marcantini

et al. 2018

Environmental Microbiology

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Biological richness is positively associated with the rates of some metabolic processes performed by microbial communities. It remains unclear, however, whether these positive associations are a general feature of the metabolic processes performed by microbial communities or whether they are specific to certain types of metabolic processes. For example, it was hypothesized that the strength of any particular positive association depends on how many different genotypes within a microbial community perform the metabolic process of interest (i.e. the 'rarity hypothesis'). We tested the generality of these positive associations by measuring the taxonomic richness, functional gene richness and rate constants for 71 different metabolic processes across 30 independent microbial communities. We found that both taxonomic and functional gene richness do indeed tend to positively associate with the rates of metabolic processes. In addition, we found that positive associations occur across a wide range of different environmental conditions. Counter to the 'rarity hypothesis', however, we did not detect a relationship between the strengths of the positive associations and the rarity of each metabolic process. Together, our data provide empirical evidence that positive associations with biological richness may indeed be a general feature of the metabolic processes performed by microbial communities.

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“…Seeking to overcome these challenges, previous studies have sequenced and functionally characterized microbial communities from different biomass-degrading environments. Examples include microbial communities from compost [ 7 – 9 ], bovine rumen [ 6 , 10 ], guts of animals [ 11 – 16 ], soil [ 17 , 18 ], and river water [ 19 ]. These studies have revealed the lignocellulolytic capabilities of microbial communities present in diverse ecosystems and the highly complex and cooperative interactions between multiple microbial species and their enzymes to achieve lignocellulose breakdown.…”

Section: Introductionmentioning

confidence: 99%

Targeted metatranscriptomics of compost-derived consortia reveals a GH11 exerting an unusual exo-1,4-β-xylanase activity

Mello

Alessi

Riaño‐Pachón

et al. 2017

Biotechnol Biofuels

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BackgroundUsing globally abundant crop residues as a carbon source for energy generation and renewable chemicals production stand out as a promising solution to reduce current dependency on fossil fuels. In nature, such as in compost habitats, microbial communities efficiently degrade the available plant biomass using a diverse set of synergistic enzymes. However, deconstruction of lignocellulose remains a challenge for industry due to recalcitrant nature of the substrate and the inefficiency of the enzyme systems available, making the economic production of lignocellulosic biofuels difficult. Metatranscriptomic studies of microbial communities can unveil the metabolic functions employed by lignocellulolytic consortia and identify novel biocatalysts that could improve industrial lignocellulose conversion.ResultsIn this study, a microbial community from compost was grown in minimal medium with sugarcane bagasse sugarcane bagasse as the sole carbon source. Solid-state nuclear magnetic resonance was used to monitor lignocellulose degradation; analysis of metatranscriptomic data led to the selection and functional characterization of several target genes, revealing the first glycoside hydrolase from Carbohydrate Active Enzyme family 11 with exo-1,4-β-xylanase activity. The xylanase crystal structure was resolved at 1.76 Å revealing the structural basis of exo-xylanase activity. Supplementation of a commercial cellulolytic enzyme cocktail with the xylanase showed improvement in Avicel hydrolysis in the presence of inhibitory xylooligomers.ConclusionsThis study demonstrated that composting microbiomes continue to be an excellent source of biotechnologically important enzymes by unveiling the diversity of enzymes involved in in situ lignocellulose degradation.Electronic supplementary materialThe online version of this article (10.1186/s13068-017-0944-4) contains supplementary material, which is available to authorized users.

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Defining the functional traits that drive bacterial decomposer community productivity

Cited by 35 publications

References 38 publications

Long-term cellulose enrichment selects for highly cellulolytic consortia and competition for public goods

Long-term cellulose enrichment selects for highly cellulolytic consortia and competition for public goods

Generality of associations between biological richness and the rates of metabolic processes across microbial communities

Targeted metatranscriptomics of compost-derived consortia reveals a GH11 exerting an unusual exo-1,4-β-xylanase activity

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