Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing

et al. 2020

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Background Microorganisms that degrade cellulose utilize extracellular processes that yield free intermediates which promote interactions with non-cellulolytic organisms. We hypothesized that these interactions determine the ecological and physiological traits governing the fate of cellulosic carbon (C) in soil. We employed metagenomic-SIP and metaproteomics to characterize the attributes of cellulolytic and non-cellulolytic microbes accessing 13C from cellulose. We hypothesized that cellulolytic taxa would exhibit competitive traits to limit access, while non-cellulolytic taxa would display metabolic dependency, such as signatures of adaptive gene loss. We tested this hypothesis by evaluating genomic traits indicative of competitive exclusion or metabolic dependency, such as antibiotic production, growth rate, surface attachment, biomass degrading potential and auxotrophy. Results The most 13C-enriched taxa were cellulolytic Cellvibrio (Gammaproteobacteria) and Chaetomium (Ascomycota), which exhibited a strategy of self-sufficiency (prototrophy), rapid growth, and competitive exclusion via antibiotic production. These ruderal taxa were common indicators of soil disturbance in agroecosystems, such as tillage and fertilization. Auxotrophy was more prevalent in cellulolytic Actinobacteria than in cellulolytic Proteobacteria, demonstrating differences in dependency among cellulose degraders. Non-cellulolytic taxa that accessed 13C from cellulose (Planctomycetales, Verrucomicrobia and Vampirovibrionales) were highly dependent, as indicated by patterns of auxotrophy and 13C-labeling (i.e. partial labelling or labeling at later-stages). Major 13C-labeled cellulolytic microbes (e.g. Sorangium, Actinomycetales, Rhizobiales and Caulobacteraceae) possessed adaptations for surface colonization (e.g. gliding motility, hyphae, attachment structures) signifying the importance of surface ecology in decomposition. Conclusions Our results demonstrate that access to cellulose was accompanied by ecological trade-offs characterized by differing degrees of metabolic dependency and competitive exclusion. These trade-offs influence microbial growth dynamics on particulate organic carbon and reveal that the fate of carbon is governed by a complex economy within the microbial community. We propose three ecological groups for microbes participating in this economy: (i) independent primary degraders, (ii) integrated primary degraders and (iii) mutualists, opportunists and parasites.

Section: Independent Primary Degradersmentioning

confidence: 78%

Competitive exclusion and metabolic dependency among microorganisms structure the cellulose economy of agricultural soil

Wilhelm¹,

et al. 2020

Preprint

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“…Cellvibrio and Devosia populations peaked earlier than any other 13 Cenriched taxa and were in decline as dependent taxa increased in relative abundance. The fungus Chaetomium exhibited similar trends of early 13 C-enrichment, occupying upwards of 20% of the 13 C-DNA pool by day 7 in a sibling study at the same eld site [42]. Chaetomium are also prototrophic, being capable of growth on cellulose in minimal media without the addition of amino acids or cofactors [43], though our methods were not validated for predicting prototrophy in eukaryotic genomes.…”

Section: Independent Primary Degradersmentioning

confidence: 90%

“…A schematic overview of the methods used in this study is presented in Figure S1. The 16S rRNA gene and ITS1 region amplicon data from this DNA-SIP experiment [11] and a sibling study [42] are available at the NCBI under BioProjects PRJNA317227 and PRJNA589050, respectively.…”

Section: Methodsmentioning

confidence: 99%

Competitive exclusion and metabolic dependency among microorganisms structure the cellulose economy of agricultural soil

Wilhelm

et al. 2020

Preprint

Self Cite

Background Microorganisms that degrade cellulose utilize extracellular processes that yield free intermediates which promote interactions with non-cellulolytic organisms. We hypothesized that these interactions determine the ecological and physiological traits governing the fate of cellulosic carbon (C) in soil. We used data from a metagenomic-SIP experiment to perform comparative genomics and characterize the attributes of cellulolytic and non-cellulolytic taxa accessing 13C from cellulose. We hypothesized that cellulolytic taxa would exhibit competitive traits to limit access, while non-cellulolytic taxa would display metabolic dependency, such as signatures of adaptive gene loss. We tested our hypotheses by evaluating genomic traits indicative of competitive exclusion or metabolic dependency, such as antibiotic production, growth rate, surface attachment, biomass degrading potential and auxotrophy.Results The most 13C-enriched taxa were cellulolytic Cellvibrio (Gammaproteobacteria) and Chaetomium (Ascomycota), which exhibited a strategy of self-sufficiency (prototrophy), rapid growth, and competitive exclusion via antibiotic production. Auxotrophy was more prevalent in cellulolytic Actinobacteria than in cellulolytic Proteobacteria, demonstrating differences in dependency among cellulose degraders. Non-cellulolytic taxa that accessed 13C from cellulose (Planctomycetales, Verrucomicrobia and Vampirovibrionales) were highly dependent, as indicated by patterns of auxotrophy and 13C-labeling (i.e. partial labelling or labeling at later-stages). Major 13C-labeled cellulolytic microbes (e.g. Sorangium, Actinomycetales, Rhizobiales and Caulobacteraceae) possessed adaptations for surface colonization (e.g. gliding motility, hyphae, attachment structures) signifying the importance of surface ecology in decomposition. Conclusions Our results demonstrate that access to cellulose was accompanied by ecological trade-offs characterized by differing degrees of metabolic dependency and competitive exclusion. These trade-offs influence microbial growth dynamics on particulate organic carbon and reveal that the fate of carbon is governed by a complex economy within the microbial community. We propose three ecological groups to describe participants in this economy: (i) independent primary degraders, (ii) integrated primary degraders and (iii) mutualists, opportunists and parasites. The relative importance and taxonomic composition of these groups reported here should be considered context dependent, likely reflecting disturbance and management practices common to agricultural soils.

“…A schematic overview of the methods used in this study is presented in Figure S1. The 16S rRNA gene and ITS1 region amplicon data from this DNA-SIP experiment [11] and a sibling study [34] are available at the NCBI under BioProjects PRJNA317227 and PRJNA589050, respectively. and a Q-Exactive HF mass spectrometer (Thermo Scientific, San Jose, CA).…”

Section: Methodsmentioning

confidence: 99%

Competitive exclusion and metabolic dependency among microorganisms structure the cellulose economy of agricultural soil

Wilhelm¹,

et al. 2020

Preprint

Self Cite

Many cellulolytic microorganisms degrade cellulose through extracellular processes that yield free intermediates which promote interactions with non-cellulolytic organisms. We hypothesize that these interactions determine the ecological and physiological traits that govern the fate of cellulosic carbon (C) in soil. We evaluated the genomic potential of soil microorganisms that access C from 13 C-labeled cellulose. We used metagenomic-SIP and metaproteomics to evaluate whether cellulolytic and non-cellulolytic microbes that access 13 C from cellulose encode traits indicative of metabolic dependency or competitive exclusion. The most highly 13 C-enriched taxa were cellulolytic Cellvibrio ( Gammaproteobacteria ) and Chaetomium ( Ascomycota ), which exhibited a strategy of self-sufficiency (prototrophy), rapid growth, and competitive exclusion via antibiotic production. These ruderal taxa were common indicators of soil disturbance in agroecosystems, such as tillage and fertilization. Auxotrophy was more prevalent in cellulolytic Actinobacteria than in cellulolytic Proteobacteria , demonstrating differences in dependency among cellulose degraders. Non-cellulolytic taxa that accessed 13 C from cellulose ( Planctomycetales , Verrucomicrobia and Vampirovibrionales ) were highly dependent, as indicated by patterns of auxotrophy and 13 C-labeling (i.e. partial labelling or labeling at later-stages). Major 13 C-labeled cellulolytic microbes ( e.g. Sorangium, Actinomycetales, Rhizobiales and Caulobacteraceae ) possessed adaptations for surface colonization ( e.g. gliding motility, hyphae, attachment structures) signifying the importance of surface ecology in decomposition. These results suggest that access to cellulose was accompanied by ecological trade-offs characterized by differing degrees of metabolic dependency and competitive exclusion. These trade-offs likely influence microbial growth dynamics on particulate organic carbon and reveal that the fate of carbon is governed by a complex economy within the microbial community.