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We didn't start the fire

4/22/2020

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Following my previous post, I will be covering some articles in the recent special issue of the Philosophical Transactions of the Royal Society B entitled "Conceptual challenges in microbial community ecology". I will try and expand on topics and connect outside work as well. This will not (at least hopefully) be a summary of the articles but my insights into the topics covering microbial ecology as a field. And if you want to read along, that previous post contains the schedule of the papers for each week.

This week's highlight is "Dormancy dynamics and dispersal contribute to soil microbiome resistance" by JW Sorensen & A Shade from Michigan State University.

Microbial composition and disturbances

All communities are constantly subjected to some type of disturbances. We learn about the gravity of these disturbances in "Intro to Ecology" courses with the famous intermediate disturbance hypothesis (IDH), popularized by JH Connell. Essentially, a disturbance occurs killing/removing individuals from the community and, thus, freeing up resources. The IDH predicts that at low disturbances, species diversity is decreased due to increased competition, leading to competitive exclusion. High disturbances, species turnover is greatest. Thus, intermediate disturbances would provide the highest species diversity in a given community.

Allison & Martiny proposed that this idea of disturbances could impact microbial communities as well; in particular, that the community composition could shift or not depending on the system's ability to either be resistant (no compositional changes), resilient (return to original composition), functionally redundant (composition change, but no functional change), or altered composition and function [1]. As a side note, Ashley Shade presented this article at a CMI conference in San Diego earlier this year referring to the Allison & Martiny paper as a "classic".

This framework is the foundation for the article by Sorensen and Shade [2], Specifically, they wished to address the mechanisms by which microbial communities could respond to a disturbance by looking at its capacity to be resistant or resilient to change. Alternatively, with high disturbances would  secondary succession lead to reassembly or recovery of the original community or would alternative stable states be possible. The authors concentrated on two mechanisms that could contribute to microbiome stability: dormancy and dispersal.

Dormancy and Dispersal and FIRE

Dormancy in bacteria is a widespread and can create an equivalent of a seed bank in microbiomes [3]. Essentially, dormant cells resuscitate to help recover local populations when resources become suitable again. Dispersal can also aid in recovery if successful immigrants can establish and support resistance and restore community composition in sensitive communities. To test these ideas, the authors utilize a super cool field site as the initial microbial community from the Centralia, a series of  coal mine, underground fires that is ongoing from 1962. The underground fires constantly spreads, warming the surface soils to variable thermal conditions. Previous work by this group showed variability among recovered soil communities that they hypothesized was from dormancy dynamics.

Using a mesocosm setup, initial microbial communities were collected from temperate soils in Centralia and split into 15 samples at 14C. After 4 weeks, 9 samples were subjected to thermal stress at 60C for 8 weeks (plus 2 more weeks for steadily increasing/decreasing temp.) before returning to 14C. Of those 9 samples, 4 of the thermal stressed communities received an inoculation from the control communities, simulating a dispersal event.
Picture
The authors look at both the "active" community and the total community using rRNA counts. Interestingly, there was a bottle effect in maintaining the mesocosms with a gradual decrease in richness over time (or is this a low frequency disturbance as predicted by the IDH?!). The thermal stress induced the desired effect of altering the community composition, with disturbed communities having increased beta-dispersion. Disturbed communities continued to shift through the time-course of the thermal stressor. During the recovery span, the disturbed (no dispersal) treatment remained distinct from the initial community while the dispersal treatment strongly suggests a mechanism to promote resilience and recovery (Figure). One question I had with this dispersal treatment was the huge influx of immigrants (0.5 mL of a 10% weight slurry) - this no longer functions as a passive dispersal mechanism, so I wonder how this would translate to the actual environment? Further, the results demonstrate that the dormancy provided little contribution to the recovery of the communities. Instead, opportunists and immigrants provided a means to recover.

Conclusions

Dispersal is a known mechanism contributing to community dynamics; however, it is often difficult to discern in microbial communities without careful experimental design [4]. Here. the authors used a highly-controlled system to examine the effects of dormancy and dispersal to a disturbance. Although dormancy was less pronounced, the authors deduce that resuscitation of thermotolerant members of the community contributed to the transitional phase of the thermal stressors by assaying the active community. Personally, I could use some more evidence here and how dormancy would pertain to community stability during this disturbance period. Further, the results in this setup, although needed to tease a part these mechanisms, make me wonder how you could extrapolate this to the natural community at Centralia. 

Papers:

1. Allison SD & Martiny JBH. (2008). Resistance, resilience, and redundancy in microbial communities. PNAS.
DOI: 10.1073/pnas.0801925105


2. Sorensen JW & Shade A. (2020). Dormancy dynamics and dispersal contribute to soil microbiome resilience. Phils Trans. R. Soc. B. 
DOI: 10.1098/rstb.2019.0255

3. Lennon JT & Jones SE. (2011). Microbial seed banks: the ecological and evolutionary implications of dormancy. Nature Reviews Microbiology.
DOI: 10.1038/nrmicro2504

4. Albright MBN, Chase AB, Martiny JBH. (2019). Experimental evidence that stochasticity contributes to bacterial composition and functioning in a decomposer community. mBio.
DOI: 10.1128/mBio.00568-19
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