We delineated members of a cellulolytic soil community using metagenomic-SIP to evaluate the ecological traits of microorganisms participating in the cellulose economy. Taxa identified as 13C-enriched and cellulolytic had larger genomes and a greater number of genes encoding carbohydrate-active enzymes, secondary metabolites, surface motility or surface attachment, and tended to have faster generation times, when compared to 13C-enriched non-cellulolytic and unenriched taxa. This evidence supports our hypothesis that the fate of cellulose carbon is mediated by ecological interdependencies among cellulolytic and non-cellulolytic taxa. Furthermore, 13C-enriched cellulolytic taxa encoded diverse endoglucanases, representing 39 different subfamilies, but no single taxon encoded more than a third of these enzymes, suggesting the potential for synergistic decomposition. Auxotrophy was common among both 13C-labeled cellulolytic and non-cellulolytic taxa, indicating that most taxa acquire essential metabolites from other community members. The average phylobin was auxotrophic for 9 of 32 pathways evaluated, though the highest levels of auxotrophy occurred among non-cellulolytic 13C-labeled taxa.
The two most abundant cellulolytic taxa in the consortium, Cellvibrio and Chaetomium, were fast-growing and self-sufficient (i.e. prototrophic), both qualities of ruderal organisms. Cellvibrio dominated access to cellulosic C in two other SIP studies of agricultural soils  and, in one of the studies, were specific to agricultural soil . The most abundant endoglucanase in our metaproteome, a GH9 from Cellvibrio, predominated in worm castings from agricultural soil (ACY24809) . Both Cellvibrio and Chaetomium are commonly more abundant in tilled versus untilled fields (Figure S9) [77–80] and, the latter in disturbed forest soils . The occurrence of Chaetomium in agroecosystems may be linked to nitrogen fertilization, given their enrichment in N-fertilized fields and wetlands [82–84]. The predominance of these ruderal cellulolytic taxa is indicative of the frequent soil disturbances in agroecosystems. Thus, it remains to be seen whether the cellulose economy of infrequently disturbed soils exhibits differing trends in the competitive exclusion or metabolic dependency reported here.
The ecological classes within the cellulose economy
Our results demonstrated that access to cellulosic carbon is mediated by trade-offs related to the capacity to produce carbohydrate-active enzymes, biosynthetic capacity, growth rate, and adaptation to colonize surfaces. Taken together our results suggest that, at least, three broad ecological groups of microorganism access 13C from cellulose: (i) fast growing, biosynthetically competent cellulolytic taxa (e.g. Cellvibrio and Devosia), (ii) slow growing, metabolically-dependent (more auxotrophic), cellulolytic taxa (e.g. Actinobacteria), and (iii) slow growing, metabolically-dependent (highly auxotrophic), non-cellulolytic taxa (e.g. Planctomycetales, Verrucomicrobia and Vampirovibrionales). Certainly, a wide range of adaptive traits will affect access to cellulose carbon during decomposition, but these three categories provide a framework we can use to dissect community interactions that affect carbon cycling.
Independent primary degraders
Bacteria in the first category are first to colonize cellulosic materials based on their cellulolytic competency, self-sufficiency and rapid growth. On average, the phylobins and representative genomes of 13C-enriched cellulolytic taxa were more prototrophic and had lower minimum generation times than their 13C-enriched non-cellulolytic counterparts, though these results were statistically insignificant due to phylogenetic and ecological diversity within groups. Cellvibrio and Devosia were among the most enriched taxon in the 13C-DNA pool (1st and 4th, respectively) and were the two most prototrophic of any genome or phylobin examined. Cellvibrio and Devosia populations peaked earlier than any other 13C-enriched taxa and were in decline as dependent taxa increased in relative abundance. The yeast Chaetomium exhibited similar trends of early 13C-enrichment, occupying upwards of 20% of the 13C-DNA pool by day 7 in a sibling study at the same field site . Chaetomium are also prototrophic, being capable of growth on cellulose in minimal media without the addition of amino acids or cofactors , though our methods (designed for prokaryotes) failed to accurately annotate eukaryotic genomes. The rapid growth and self-sufficiency of Cellvibrio and Chaetomium were coupled with a strategy of competitive exclusion via the production of antibiotics such as bacteriocin, likely a cellvibriocin , and fungicides [87–89]. We expect the competitive nature of these early colonizers and their metabolic by-products to influence the ability of non-cellulolytic taxa to access cellulosic C.
Integrated primary degraders
Bacteria in the second category, primarily Actinobacteria but also Herpetosiphon (Chloroflexi), were cellulolytic but exhibited higher levels of auxotrophy and SM production than early colonists. Populations of Actinobacteria lagged in comparison to Cellvibrio, with the first signs of 13C-labelling appearing at day 14, and populations did not increase consistently over time. These trends suggest a greater integration with other population that exert top down (mortality driven) or bottom up (nutrient limitation as a result of competition for nutrients) control. Actinobacteria encoded and produced the greatest number of SMs and SM peptides, including an abundance of terpenoids which can function in interspecific signaling in soil, potentially facilitating mutualistic interactions . The potential benefit of metabolic dependency for cellulolytic Actinobacteria was apparent in their consistent auxotrophy for four of the costliest non-aromatic amino acids to synthesize, namely: isoleucine (ranked 1st ), leucine (2nd ), methionine (3rd ) and lysine (4th ) [91, 92]. We hypothesize, based on their cellulolytic capacity; SM production, and high degree of auxotrophy, that the fitness of integrated primary degraders depends on community interactions.
Mutualists, opportunists and parasites
The third ecological group we observed, the ‘MOP,’ were metabolically dependent, late-stage colonizers of cellulose, characterized by the inability to degrade cellulose and high levels of auxotrophy. The MOP were comprised of Planctomycetales, Vampirovibrionales, and Verrucomicrobia (Luteolibacter, Candidatus Xiphinematobacter and 01D2Z36), which reached maximal relative abundance after Cellvibrio, Devosia and Chaetomium, and remained abundant even after their decline. This pattern suggests dependence on products of community metabolism either through co-metabolism, the consumption of metabolic by-products or the consumption of macromolecules released during the turnover of microbial biomass. Indeed, these taxa all have traits that indicate lifestyles characterized by dependency on other microorganisms.
Planctomyces are commonly found to colonize the surfaces of marine algae, and to metabolize forms of algal polysaccharides, but not cellulose [93–95]. They purportedly assimilate oligosaccharides into their cells, indicating the ability to scavenge higher molecular weight degradation by-products [13, 96–98]. The capacity of Planctomyces to attach to surfaces with holdfast, and their distinct tolerance to a range of antibiotics, would advantage an opportunistic lifestyle, particularly amongst antibiotic-producing primary degraders [95, 99, 100]. Cultured representatives for two other highly auxotrophic 13C-enriched non-cellulolytic phylobins are obligate symbionts, namely Vampirovibrio and Candidatus Xiphinematobacter. The former are algal parasites that encode a range of GHs  but lack endoglucanases, and the latter are endobionts of nematodes, and are commonly observed in forest litter, cellulose-degrading consortia or in associated with Basidiomycota [102–105].
One set of phylobins provided evidence for what could be considered opportunistic ‘cheating’ . Phylobins from Sphingomonadales differed in terms of weak and strong 13C-enrichment yet shared the same pattern of auxotrophy. The strongly enriched phylobins encoded several endoglucanases and bacteriocins, while the equally sized weakly-enriched phylobins lacked these capabilities. These data suggest that the strongly labeled cellulolytic strain is degrading 13C-cellulose extracellularly and the weakly 13C-enriched strain can access degradation products as well as other sources of unlabeled carbon present in soil. The capacity of Sphingomonas species to degrade cellulose through the activity of extracellular enzymes is known [106, 107].
The role of surface ecology in decomposition
Several major populations of microbes that accessed 13C from cellulose were capable of surface-adherence and/or surface-motility. Genes encoding surface attachment were present in phylobins, or have been previously reported, in Rhizobiaceae (Ensifer/Sinorhizobium, Rhizobium and Agrobacterium), Hyphomicrobiaceae (Devosia), Sphingomonadaceae (Sphingomonas) and Caulobacteraceae (Asticcacaulis, Brevundimonas and Caulobacter), as well as in Pseudoxanthomonas and Planctomycetaceae (Planctomyces and Rhodopirellula) [108–110]. Each of these genera, except for those in Planctomyceteceae, are represented by isolates capable of degrading cellulose [111–118]. For these organisms, attachment would provide preferential access to the by-products of cellulose degradation. This phenomenon is exemplified by the abundance of sugar transporters located on the stalk used by Caulobacter to adhere to surfaces [119, 120]. Attachment may also facilitate cooperation to crowd out competitors from accessing resources, as observed in the social behavior of Caulobacter during xylan degradation (D’Souza et al., bioRxiv pre-print available soon) or in the coordination of extracellular degradative processes by surface-gliding bacteria Herpetosiphon and Sorangium [121, 122]. Social interactions and cell aggregation density were critical determinants of the rate and efficiency of decomposition of particulate carbon . The dynamics of surface attachment have ramifications for ecology and evolution as well as biogeochemical cycling, which have yet been studied outside of the rumen [123, 124].
Diversity at the sub-genus level in the cellulose economy
Shotgun metagenomics provided a comprehensive view of the cellulolytic consortium but was ineffective at resolving the genomes of closely related species. Phylobins were comprised of large pangenomes which limited our ability to test for adaptive gene loss among closely related species, known to be important in the evolution of metabolic dependencies [20, 125]. The recovery of large single-genus phylobins for Myxococcales (Sorangium), Cellvibrionales (Cellvibrio), Planctomycetales (Planctomyces) and Micrococcales (Microbacterium), provided evidence of sizeable pangenomic genetic diversity which could reflect niche partitioning among close relatives. However, the degree of 13C-enrichment within these single-genus phylobins did not differ, except for Planctomycetales and Sphingomonadales (i.e. ‘weak’ versus ‘strong’ phylobins). We conclude that few differences in the capacity to access cellulosic carbon had occurred among closely related populations.