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

2020 ◽  
Author(s):  
Roland C Wilhelm ◽  
Charles Pepe-Ranney ◽  
Pamela Weisenhorn ◽  
Mary Lipton ◽  
Daniel H. Buckley

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.

2020 ◽  
Author(s):  
Roland C Wilhelm ◽  
Charles Pepe-Ranney ◽  
Pamela Weisenhorn ◽  
Mary Lipton ◽  
Daniel H. Buckley

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.


2020 ◽  
Author(s):  
Roland C Wilhelm ◽  
Charles Pepe-Ranney ◽  
Pamela Weisenhorn ◽  
Mary Lipton ◽  
Daniel H. Buckley

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.


mBio ◽  
2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Roland C. Wilhelm ◽  
Charles Pepe-Ranney ◽  
Pamela Weisenhorn ◽  
Mary Lipton ◽  
Daniel H. Buckley

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.


2017 ◽  
Vol 2 ◽  
pp. 32 ◽  
Author(s):  
Simon Gras ◽  
Allison Jackson ◽  
Stuart Woods ◽  
Gurman Pall ◽  
Jamie Whitelaw ◽  
...  

Background: Micronemal proteins of the thrombospondin-related anonymous protein (TRAP) family are believed to play essential roles during gliding motility and host cell invasion by apicomplexan parasites, and currently represent major vaccine candidates against Plasmodium falciparum, the causative agent of malaria. However, recent evidence suggests that they play multiple and different roles than previously assumed. Here, we analyse a null mutant for MIC2, the TRAP homolog in Toxoplasma gondii. Methods: We performed a careful analysis of parasite motility in a 3D-environment, attachment under shear stress conditions, host cell invasion and in vivo virulence. Results: We verified the role of MIC2 in efficient surface attachment, but were unable to identify any direct function of MIC2 in sustaining gliding motility or host cell invasion once initiated. Furthermore, we find that deletion of mic2 causes a slightly delayed infection in vivo, leading only to mild attenuation of virulence; like with wildtype parasites, inoculation with even low numbers of mic2 KO parasites causes lethal disease in mice. However, deletion of mic2 causes delayed host cell egress in vitro, possibly via disrupted signal transduction pathways. Conclusions: We confirm a critical role of MIC2 in parasite attachment to the surface, leading to reduced parasite motility and host cell invasion. However, MIC2 appears to not be critical for gliding motility or host cell invasion, since parasite speed during these processes is unaffected. Furthermore, deletion of MIC2 leads only to slight attenuation of the parasite.


2017 ◽  
Vol 2 ◽  
pp. 32 ◽  
Author(s):  
Simon Gras ◽  
Allison Jackson ◽  
Stuart Woods ◽  
Gurman Pall ◽  
Jamie Whitelaw ◽  
...  

Background: Micronemal proteins of the thrombospondin-related anonymous protein (TRAP) family are believed to play essential roles during gliding motility and host cell invasion by apicomplexan parasites, and currently represent major vaccine candidates against Plasmodium falciparum, the causative agent of malaria. However, recent evidence suggests that they play multiple and different roles than previously assumed. Here, we analyse a null mutant for MIC2, the TRAP homolog in Toxoplasma gondii. Methods: We performed a careful analysis of parasite motility in a 3D-environment, attachment under shear stress conditions, host cell invasion and in vivo virulence. Results: We verified the role of MIC2 in efficient surface attachment, but were unable to identify any direct function of MIC2 in sustaining gliding motility or host cell invasion once initiated. Furthermore, we find that deletion of mic2 causes a slightly delayed infection in vivo, leading only to mild attenuation of virulence; like with wildtype parasites, inoculation with even low numbers of mic2 KO parasites causes lethal disease in mice. However, deletion of mic2 causes delayed host cell egress in vitro, possibly via disrupted signal transduction pathways. Conclusions: We confirm a critical role of MIC2 in parasite attachment to the surface, leading to reduced parasite motility and host cell invasion. However, MIC2 appears to not be critical for gliding motility or host cell invasion, since parasite speed during these processes is unaffected. Furthermore, deletion of MIC2 leads only to slight attenuation of the parasite.


Author(s):  
Wei Qi ◽  
Mengyi Sha ◽  
Shanling Li

Problem definition: We develop a crossdisciplinary analytics framework to understand citywide mobility-energy synergy. In particular, we investigate the potential of shared autonomous electric vehicles (SAEVs) for improving the self-sufficiency and resilience of solar-powered urban microgrids. Academic/practical relevance: Our work is motivated by the ever-increasing interconnection of energy and mobility service systems at the urban scale. We propose models and analytics to characterize the dynamics of the SAEV-microgrid service systems, which were largely overlooked by the literature on service operations and vehicle-grid integration (VGI) analysis. Methodology: We develop a space-time-energy network representation of SAEVs. Then, we formulate linear program models to incorporate an array of major operational decisions interconnecting the mobility and energy systems. To preventatively ensure microgrid resilience, we also propose an “N − 1” resilience-constrained fleet dispatch problem to cope with microgrid outages. Results: Combining eight data sources of New York City, our results show that 80,000 SAEVs in place of the current ride-sharing mobility assets can improve the microgrid self-sufficiency by 1.45% (benchmarked against the case without grid support) mainly via the spatial transfer of electricity, which complements conventional VGI. Scaling up the SAEV fleet size to 500,000 increases the microgrid self-sufficiency by 8.85% mainly through temporal energy transfer, which substitutes conventional VGI. We also quantify the potential and trade-offs of SAEVs for peak electricity import reduction and ramping mitigation. In addition, microgrid resilience can be enhanced by SAEVs, but the actual resilience level varies by microgrids and by the hour when grid contingency occurs. The SAEV fleet operator can further maintain the resilience of pivotal microgrid areas at their maximum achievable level with no more than a 1% increase in the fleet repositioning trip length. Managerial implications: Our models and findings demonstrate the potential in deepening the integration of urban mobility and energy service systems toward a smart-city future.


2019 ◽  
Author(s):  
Winka Le Clec’h ◽  
Robbie Diaz ◽  
Frédéric D. Chevalier ◽  
Marina McDew-White ◽  
Timothy J.C. Anderson

ABSTRACTBackgroundParasite traits associated with transmission success, such as the number of infective stages released from the host, are expected to be optimized by natural selection. However, in the trematode parasite Schistosoma mansoni, a key transmission trait – the number of cercariae larvae shed from infected Biomphalaria spp. snails – varies significantly within and between different parasite populations and selection experiments demonstrate that this variation has a strong genetic basis. In this study, we compared the transmission strategies of two laboratory schistosome population and their consequences for their snail host.MethodsWe infected inbred Biomphalaria glabrata snails using two Schistosoma mansoni parasite populations (SmBRE and SmLE), both isolated from Brazil and maintained in the laboratory for decades. We compared life history traits of these two parasite populations by quantifying sporocyst growth within infected snails (assayed using qPCR), output of cercaria larvae, and impact on snail host physiological response (i.e. hemoglobin rate, laccase-like activity) and survival.ResultsWe identified striking differences in virulence and transmission between the two studied parasite populations. SmBRE (low shedder (LS) parasite population) sheds very low numbers of cercariae, and causes minimal impact on the snail physiological response (i.e. laccase-like activity, hemoglobin rate and snail survival). In contrast, SmLE (high shedder (HS) parasite population) sheds 8-fold more cercariae (mean ± se cercariae per shedding: 284±19 vs 2352±113), causes high snail mortality, and has strong impact on snail physiology. We found that HS sporocysts grow more rapidly inside the snail host, comprising up to 60% of cells within infected snails, compared to LS sporocysts which comprised up to 31%. Cercarial production is strongly correlated to the number of S. mansoni sporocyst cells present within the snail host tissue, although the proportion of sporocyst cells alone does not explain the low cercarial shedding of SmBRE.ConclusionsWe demonstrated the existence of alternative transmission strategies in the S. mansoni parasite consistent with trade-offs between parasite transmission and host survival: a “boom-bust” strategy characterized by high virulence, high transmission and short duration infections and a “slow and steady” strategy with low virulence, low transmission but long duration of snail host infections.


2021 ◽  
Vol 13 (6) ◽  
pp. 3190
Author(s):  
Paresh B. Shirsath ◽  
Pramod K. Aggarwal

Climate-smart agriculture targets integrated adaptation and mitigation strategies for delivering food security and greenhouse gas emissions reduction. This study outlines a methodology to identify the trade-offs between food production, emissions, and income under technology and food demand-shift scenario and climate change. The methodology uses Climate Smart Agricultural Prioritization (CSAP) toolkit a multi-objective land-use allocation model, and detailed databases, characterizing the agricultural production processes at the land-unit scale. A case study has also been demonstrated for Bihar, a state in India. The quantification of trade-offs demonstrates that under different technology growth pathways alone the food self-sufficiency for Bihar cannot be achieved whilst the reduction in emission intensity targets are achievable up to 2040. However, both food self-sufficiency and reduction in emission intensity can be achieved if we relax constraints on dietary demand and focus on kilo-calories maximization targets. The district-level analysis shows that food self-sufficiency and reduction in emission intensity targets can be achieved at a local scale through efficient crop-technology portfolios.


Author(s):  
A. Whitney Sanford

This chapter illustrates how intentional communities translate their bundled values of nonviolence, self-sufficiency, equity, and voluntary simplicity through producing and consuming food. These communities ask what constitutes violence in terms of food and make choices that accord with their specific contexts, goals and geographies, e.g., local vs organic. Catholic worker houses must balance goals of hospitality to the poor with their goals of sustainability. Food rescue helps them combat waste and feed the poor. Whether to eat meat and communal eating become two areas of tension in communities. This chapter explores first, how these communities perform these bundled values in their food practices, including what they eat, what they grow, and what they purchase or gather; and second, the processes and trade-offs of practicing these values.


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