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

Abstract 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.

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

10.21203/rs.2.23522/v2 ◽

2020 ◽

Author(s):

Roland C Wilhelm ◽

Charles Pepe-Ranney ◽

Pamela Weisenhorn ◽

Mary Lipton ◽

Daniel H. Buckley

Keyword(s):

Competitive Exclusion ◽

Antibiotic Production ◽

Growth Dynamics ◽

Soil Disturbance ◽

Gliding Motility ◽

Ecological Groups ◽

Surface Attachment ◽

Trade Offs ◽

Self Sufficiency ◽

Attachment Structures

Abstract 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.

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

10.21203/rs.3.rs-26792/v1 ◽

2020 ◽

Author(s):

Roland C Wilhelm ◽

Charles Pepe-Ranney ◽

Pamela Weisenhorn ◽

Mary Lipton ◽

Daniel H. Buckley

Keyword(s):

Management Practices ◽

Competitive Exclusion ◽

Agricultural Soils ◽

Antibiotic Production ◽

Growth Dynamics ◽

Taxonomic Composition ◽

Gliding Motility ◽

Ecological Groups ◽

Trade Offs ◽

Attachment Structures

Abstract 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.

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Competitive Exclusion and Metabolic Dependency among Microorganisms Structure the Cellulose Economy of an Agricultural Soil

mBio ◽

10.1128/mbio.03099-20 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Roland C. Wilhelm ◽

Charles Pepe-Ranney ◽

Pamela Weisenhorn ◽

Mary Lipton ◽

Daniel H. Buckley

Keyword(s):

Stable Isotope ◽

Competitive Exclusion ◽

Antibiotic Production ◽

Stable Isotope Probing ◽

Gliding Motility ◽

Interspecies Interactions ◽

Surface Attachment ◽

Soil Microbial ◽

Trade Offs ◽

Attachment Structures

ABSTRACT Microorganisms that degrade cellulose utilize extracellular reactions that yield free by-products which can promote interactions with noncellulolytic organisms. We hypothesized that these interactions determine the ecological and physiological traits governing the fate of cellulosic carbon (C) in soil. We performed comparative genomics with genome bins from a shotgun metagenomic-stable isotope probing experiment to characterize the attributes of cellulolytic and noncellulolytic taxa accessing 13C from cellulose. We hypothesized that cellulolytic taxa would exhibit competitive traits that limit access, while noncellulolytic taxa would display greater 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. 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. Noncellulolytic taxa that accessed 13C from cellulose (Planctomycetales, Verrucomicrobia, and Vampirovibrionales) were also more dependent, as indicated by patterns of auxotrophy and 13C labeling (i.e., partial labeling 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 decomposing particulate organic matter. Our results demonstrated that access to cellulosic C was accompanied by ecological trade-offs characterized by differing degrees of metabolic dependency and competitive exclusion. IMPORTANCE Our study reveals the ecogenomic traits of microorganisms participating in the cellulose economy of soil. We identified three major categories of participants in this economy: (i) independent primary degraders, (ii) interdependent primary degraders, and (iii) secondary consumers (mutualists, opportunists, and parasites). Trade-offs between independent primary degraders, whose adaptations favor antagonism and competitive exclusion, and interdependent and secondary degraders, whose adaptations favor complex interspecies interactions, are expected to affect the fate of microbially processed carbon in soil. Our findings provide useful insights into the ecological relationships that govern one of the planet’s most abundant resources of organic carbon. Furthermore, we demonstrate a novel gradient-resolved approach for stable isotope probing, which provides a cultivation-independent, genome-centric perspective into soil microbial processes.

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