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Cellulose as a public good

1/27/2021

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For this week, I will be reading the paper out of the Buckley group entitled:
"Competitive Exclusion and Metabolic Dependency among Microorganisms Structure the Cellulose Economy of an Agricultural Soil" in mBio

I am pretty excited for this one as it kinda perfectly blends my passion for soil science (and C cycling) and the production of specialized metabolites (like antibiotics). Let's get this going!

Cellulases and leaf litter decomposition

Picture
Figure 1. Composition of leaf litter from a variety of ecosystems along an elevation gradient [1]
The top layer of soil, otherwise known as the leaf litter layer, is decaying plant debris that can be utilized by the resident microbial community. Typically, this leaf litter layer is comprised of recalcitrant, polymeric carbohydrates (Figure 1) that are difficult for bacteria to digest and incorporate into the cell. Therefore, bacteria need to release extracellular enzymes to bind to the primary source of carbohydrates and break them down to smaller byproducts before they can be used for cellular metabolism
Bacteria that encode these cellulases are pretty well-distributed across the bacterial domain; however, many of the analyzed genomes lack complete degradation pathways for cellulose utilization [2]. While this is great to know the phylogenetic distribution of known cellulose degraders, a comparitive genomics perspective is limited as it cannot relate the genomic potential to  community dynamics. This is where the field of carbon utilization is super amazing!
Recently, research groups have applied some laboratory techniques to couple stable isotope probing (SIP), flow cytometry, and shotgun metagenomics. For instance, a recent paper from JGI used a "cellulose hook" (Figure 2) to recruit microbes to fluorescently labeled cellulose particles and then sorted them based on that fluorescent to sequence single cell genomes [3]. Seriously, how cool is that?! They can actually target active cellulose degraders in their system and sequence for their genomic potential. In the case of this paper, "​species-level organism with novel and phylogenetically distinct cellulolytic activity"
Picture
Fluorescent substrate strategy used to identify microbes that colonize crystalline cellulose particles [3]

Physiological trade-offs

Now that we have a brief background, let's dive in. Just a reminder that bacteria reside in communities. Meaning bacteria will have different life-history strategies like being a cellulose degrader. But if your neighbor is already releasing the enzymes to break down the cellulose, why would other bacteria need to also release MORE cellulases that require investment by the cell to produce and excrete. This means we can have a range of "cellulose utilizers" ranging from primary (and independent from other bacteria) degraders, incomplete cellulase degraders (only encoding some of the pathway), and opportunistic cheaters (who just gobble up the byproducts). This is where a major thought experiment can be underway and we can ask:
Why invest in extracellular enzyme production if others are just going to cheat? In other words, how does the bacteria "guarantee" a return on its investment?
Hint: antibiotics!!!

Main results

The authors [4] use [13C]cellulose to group bacterial soils into a gradient of cellulose incorporation and used shotgun metagenomics to construct MAGs (metagenome assembled genomes). As the authors note, the MAGs were unable to recover abundant organisms and used a higher-level binning into "phylobins" at the Order level, as a side note they justify this by as the traits should be conserved at a phylogenetic level. Unsurprisingly, certain phylobins were enriched in [13C]cellulose while others were not. To get at the mechanisms driving these observations, the authors selected a representative genome (a bit unclear on this part - anyone want to help?) to compare the genomes for genomic traits, including genes related to surface attachment, motility, and specialized metabolism. 

[Funny result: the phylobin Cellulomonas was NOT enriched by ​[13C]cellulose.]
The authors find that [13C]cellulose enriched phylobins produce more carbohydrate-active enzymes and more antibiotics, suggesting an ecological trade-off. One question here is: there is a general physiological trade-off in growth v yield. However, the authors note here that the [13C]cellulose-enriched taxa do both, grow faster AND make the investment in extracellular molecules, including both carbohydrate-active enzymes and specialized metabolites. 

Outstanding questions:

1. How were the SM gene clusters linked to the proteomics? I am not familiar with proteomics at all, so generally curious how this was done.
2. What are the advantages of the slower growing, non-cellulolytic bacteria? If they cannot digest the substrate nor grow faster than the degraders, how do they persist in the community?

Anyone have additional thoughts???

Papers:

1. Chase AB, Gomez-Lunar Z, Lopez AE, Li J, Allison SD, Martiny AC, Martiny JBH. (2018). Emergence of soil bacterial ecotypes along a climate gradient. Environmental Microbiology
DOI: 10.1111/1462-2920.14405

​2. Berlemont R, Martiny AC. (2012). Phylogenetic distribution of potential cellulases in bacteria. Applied and Environmental Microbiology
DOI: ​10.1128/AEM.03305-12

3. Doud DFR, Bowers RM, Schulz F, De Raad M, Deng K, Tarver A, Glasgow E, Meulen KV, Fox B, Deutsch S, Yoshikuni Y, Northen T, Hedlund BP, Singer SW, Ivanova N, Woyke T. (2020). Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere. The ISME Journal
DOI: 10.1038/s41396-019-0557-y

4. Wilhelm RC, Pepe-Ranney C, Weisenhorn P, Lipton M, Buckley DH. (2021). Competitive exclusion and metabolic dependency among microorganisms structure the cellulose economy of an agricultural soil. mBio
DOI: 10.1128/mBio.03099-20
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