Impact of Microorganisms

TWiM #310: Starvation vs. Dehydration—Who Loses, Who Wins?

Podcast and Annotation Information
  • Annotation by Sophie Corley, Isabelle Martin, Urmila Shanmugam, and Michaela Gazdik Stofer.
  • Podcast audio by TWiM: Listen to TWiM #310 Podcast
  • Podcast transcript by Otter.ai and edited by Marvin Romo, Harshita Sharma: Access Podcast Transcripts
  • Papers Discussed:
    • Yilmaz B, Fuhrer T, Morgenthaler D, Krupka N, Wang D, Spari D, Candinas D, Misselwitz B, Beldi G, Sauer U, Macpherson AJ. Plasticity of the adult human small intestinal stoma microbiota. Cell Host Microbe. 30(12):1773-1787. doi: 10.1016/j.chom.2022.10.002
    • Imminger S, Meier DV, Schintlmeister A, Legin A, Schnecker J, Richter A, Gillor O, Eichorst SA, Woebken D. 2024. Survival and rapid resuscitation permit limited productivity in desert microbial communities. Nat Commun. 15(1):3056. doi: 10.1038/s41467-024-46920-6.

1. Paper Abstracts

1.1. Snippet paper; discussion starts at 1:44 minutes

The Most Interesting Things (according to students)

Most gut microbiome papers talk about the GI microbiome but they are really sampling the colon microbiome. This is an interesting distinction that I didn’t realize before. Stoma bags are used to replace the colon in certain diseases. It was interesting that the researchers used this patient population to develop a new way of collecting the gut microbes for analysis.

The abstract cannot be copied due to licensing restrictions. Elsevier user license: used for Elsevier open archive, which makes the final published article from certain journals free to read after an embargo period. Not able to be used for commercial or non-commercial purposes. Please see licensing information and links to the article at the journal’s web page and/or PubMed in Section 8.1.

1.2. Main paper; discussion starts at 19:10 minutes

The Most Interesting Things (according to students)

It was very interesting that they used a new technique (nanoSIMS) to look at the metabolic activity that was going on in a single cell; that it is possible to analyze compounds and metabolites from one single bacterial cell. It was also interesting to see how metabolism changed with the rain in the desert; that microbes are able to survive in very dry deserts by regulating their metabolic activity to have limited productivity. When it rained they would have short periods of activity where they focused on repair instead of growing rapidly.

“Microbial activity in drylands tends to be confined to rare and short periods of rain. Rapid growth should be key to the maintenance of ecosystem processes in such narrow activity windows, if desiccation and rehydration cause widespread cell death due to osmotic stress. Here, simulating rain with 2H2O followed by single-cell NanoSIMS, we show that biocrust microbial communities in the Negev Desert are characterized by limited productivity, with median replication times of 6 to 19 days and restricted number of days allowing growth. Genome-resolved metatranscriptomics reveals that nearly all microbial populations resuscitate within minutes after simulated rain, independent of taxonomy, and invest their activity into repair and energy generation. Together, our data reveal a community that makes optimal use of short activity phases by fast and universal resuscitation enabling the maintenance of key ecosystem functions. We conclude that desert biocrust communities are highly adapted to surviving rapid changes in soil moisture and solute concentrations, resulting in high persistence that balances limited productivity.” (Imminger et al 2024, no changes)

2. Vision and Change Core Concepts and 2024 ASM Fundamental Statements

Snippet Main
Vision and Change Topics
  • Microbial Ecology (V&C_ME)
  • Structure and Function (V&C_SF)
  • Evolution (V&C_E)
  • Impact of Microorganisms (V&C_IM)
  • Metabolic Pathways (V&C_MP)
ASM Fundamental Statements
  • Fundamental Statement 7 (ASM_7): Microbes have evolved structures adapted for specific functions that are often associated with a fitness advantage in a particular environment.
  • Fundamental Statement 20 (ASM_20): Microbes are ubiquitous, found in diverse and dynamic ecosystems, where they use available resources and often form complex communities.
  • Fundamental Statement 23 (ASM_23): The health of the environment and all organisms (microbes, plants, humans, other animals) are closely linked and interdependent, as described by the One Health paradigm.
  • Fundamental Statement 3 (ASM_3): The evolution of microbes is impacted by their interactions with the environment and a variety of ecological forces, including other microbes, humans, and habitats.
  • Fundamental Statement 13 (ASM_13): Intrinsic factors, such as genotype, metabolism, and cell structures, impact the survival and growth of microbes.
  • Fundamental Statement 27 (ASM_27): The extent of microbial diversity is largely unknown, and exploration of this diversity is critical to understanding microbes and their role in the biosphere.

3.  Potential Learning Objectives for the Podcast

The student will be able to: Paper1 Order2
  • Identify different sampling methods for the small intestine and colon microbiome.
  • Recall how intestinal environments and/or microbiome populations differ along the gastrointestinal tract.
 S L
  • Predict how intestinal microbe populations might react to different food consumption levels.
 S H
  • Define biocrust.
  • Describe the role of desert microbes in ecosystem resilience.
 M L
  • Predict the significance of which metabolic processes are prioritized following rapid resuscitation processes in desert microbial communities.
 M H

1 Papers: Snippet (S) or Main (M)

2 Learning Objectives: Lower Order or Higher Order (H)

4. Techniques Described (with Time Stamps)

Here is a link to a bio-dictionary that has many, but not all definitions if you need a definition: Explore Biology Bio-Dictionary

4.1. Snippet Paper

  • Sample Collection–Small Intestine (7:22–7:53): There are many kinds of sampling techniques.  Here people swallow capsules which are open to the small intestine but then close to sample. The capsules are then retrieved from the feces. This sampling technique does not always work perfectly, but it is a start.
  • Microbiota Sampling–Stoma Bag (1:44–4:55; 10:00- 11:18): People who have their colon or parts of their colon removed (often due to inflammatory disorders) have it replaced with an ileostoma or stoma bag. Researchers used the stoma opening to collect the contents of what would be entering the small intestine. They were able to sample the contents of the bag which provided a much less invasive way of collecting samples rather than surgery or removing part of the small intestine.

4.2. Main Paper

  • Single-Cell Nanoscale Secondary Ion Mass Spectroscopy (NanoSIMS) (23:41–26:10):  Single-Cell Nanoscale Secondary Ion Mass Spectroscopy is a type of mass spectrometry that analyzes the composition of materials at a nanoscale level. It uses deuterated heavy water and creates a 50 nm window to analyze microbial cell functions.
  • Genome Resolved Metatranscriptomic Analysis (27:04–28:30): This technique uses genome and transcriptome data to inform the other.  Here, the genome of the desert microbiome population was analyzed and evaluated against gene expression data to determine the function of each species of microbe present.

5. Connections to General Microbiology Processes/Concepts (with Time Stamps)

5.1. Snippet Paper

  • Human Microbiome (1:44–11:18): This study examines the plasticity of the microbiota within the small intestine and its wide range of environments. The human microbiome is discussed and how we actually have several, but that the one people usually talk about is the colon. However, the small intestine has its own microbiome with different species of microbes due to changing environmental factors like pH and oxygen levels.
  • Microbial Metabolism, Ecology, Fermentation (14:19–15:12) : Food does not spend very long in the small intestine. The large intestine is a fermentative environment so the things that do not get absorbed in the small intestine must go through the more complicated process of fermentation in the large intestine.

5.2. Main Paper

  • Microbial Metabolism, Ecology, Carbon Cycle (19:10–22:25; 31:10–37:52 ): Desert microbes enrich the soil with carbon and nitrogen while at the same time facilitating the prevention of soil erosion and the retention of water that the soil in dry lands can possess. In order to rehydrate, the biocrust cells acquire carbon energy to grow the microbiome population.
  • Microbial Genetics, Gene Expression, DNA Repair (28:30–30:40) : With the limited rainfall, only a small portion of the desert cells were able to double so they do not put their energy into dividing, they put it into saving up for the next drought. They are using any available water to repair their genetic material and make storage compounds that will get them through the next dry period, as well as getting rid of free radicals.

6. Podcast Questions

  1. What sampling method is being explored to access the small intestine microbiome without surgery?
    1. Swallowing sampling capsules
    2. Endoscopy
    3. Urine analysis
    4. Stool samples
  2. How does the microbial community in the small intestine likely respond to periods of high food consumption?
    1. It will experience a temporary decrease in diversity with higher aerobe abundance.
    2. It will experience a temporary increase in abundance and species composition.
    3. It will experience a prolonged period of decline followed by a period of stability.
    4. There will be no significant changes as the microbiome composition is quite stable.
  3. What environmental change occurs through the gastrointestinal tract as you travel from the stomach to the small intestine to the colon that has a large effect on the microbial population?
    1. Oxygen levels and blood vessel surfaces steadily increase.
    2. The environment changes from aerobic to an anaerobic one.
    3. Enzyme activity decreases due to limited metal availability.
    4. The pH gradually lowers leading to stomach acid buildup.
  4. The biocrust is _______ (pick all that apply).
    1. important to prevent soil erosion.
    2. present in dry, desert regions.
    3. the top millimeters of the earth.
    4. enriches the soil with carbon.
    5. enriches the soil with sulfur.
  5. What role do desert microbes play in desert ecosystem resiliency?
    1. They do not play a role in the ecosystem resilience.
    2. They increase competition amongst plant species.
    3. They limit to soil erosion due to burrowing insects.
    4. They cycle nutrients including carbon and nitrogen.
  6. The researchers identified the biological processes used by desert bacteria during initial rehydration.  What are they and what do this imply?
    1. Cell division; rapid growth and colony formation  is the primary goal after rehydration.
    2. DNA repair and energy generation; survival and recovery  are crucial for persistence.
    3. Photosynthesis; replenishing depleted stores of energy and sugar are important.
    4. Bioluminescence; competition for resources is intense among desert microbes.

7. Figure Reading Exercises

The following are two figure reading exercises, both from the main paper (Figures 2EF and 7)

7.1. First Figure Reading Exercise

7.1.1. Learning Objectives

Students will be able to:

  • Identify key features in the data visualizations related to interpreting these experiments.
  • Analyze the data to identify growth differences between autotrophs, heterotrophs, and cyanobacteria.
  • Evaluate how differences in microbial replication times might influence the resilience and stability of biocrust ecosystems in response to environmental changes.
  • Evaluate the data to make conclusions about the relationship of biomass generation and cell structural changes during hydration.
Experimental Background (Imminger et al., Figure 2EF)

Biocrusts are critical for stabilizing soils and driving nutrient cycling in arid ecosystems, making it essential to understand how microorganisms found in the biocrust respond to rare and sudden hydration events.  To investigate how a hydration event affects different ecosystem growth measures for the species types that populate these arid environments,  Imminger et al. (2024) first quantified biomass generation at different timepoints after a hydration event for heterotrophic and autotrophic bacteria, as well as cyanobacteria.   Recall that autotrophs and heterotrophs differ in their metabolic needs.  The other ecosystem growth measure they investigated was replication time.  They analyzed the distribution of replication time for heterotrophic and autotrophic bacteria (panel f).

A box plot and bar chart showing biomass generation rate of bacteria based on hydration time and replication time. Heterotrophs see the most distribution 0-10 days in, but do not generate biomass over hours. Autotrophs see less biomass after hydration, and less distribution over days. Cyanobacteria sees highest biomass generation after hydration.
Figure 2. “Microbial activity detected through cellular incorporation of 2H and NanoSIMS analysis. … e Calculated biomass generation rates, inferred from NanoSIMS measurement data of single cells after different incubation times (and classified as active, shown in (b) and (c)), assuming either a heterotrophic (left panel) or chemoautotrophic (central panel) physiology and of photoautotrophic cyanobacterial filaments (right panel). Outliers are not displayed. f Histogram visualizing the frequency of replication times of single cells based on the assumption that all cells exhibit either a heterotrophic or chemoautotrophic physiology. Smoothened lines indicate kernel density estimates. Displayed data are based on the 24 h incubation sample and cover 91% (assumed heterotrophic physiology) and 72% (assumed chemoautotrophic physiology) of cells exhibiting replication times up to 40 days. The inset depicts the fractions of cells that potentially replicate in 1, 2, and 3 days. … The boxes in (…e) comprise the 2nd and 3rd quartiles with the horizontal line indicating the median. Whiskers maximally extend to 1.5 times the inter-quartile range. “(Imminger et al 2024, cropped image and edited text to include only panels e and f).

 

7.1.2. Questions

  1. A box plot (panel e) shows many statistical features including median and quartiles.  Match each feature with its description. (1 = median; 2 = mean; 3 = standard deviation; 4 = 2nd-3rd quartile; 5 = 1.5x the quartile range)
    1. ____ the horizontal line inside the box
    2. ____ the range from the upper part of the box to the lower part of the box
    3. ____ the whiskers
  2. Which species shows the greatest biomass generation?  What is your evidence?
    1. heterotrophs; the blue histogram is highest for them, as shown in panel e
    2. autotrophs; the box plot in panel d shows a small box indicating low variability
    3. cyanobacteria; the box plot in panel d shows a higher median at 12 hours
  3. What does the autotroph biomass generation rate after hydration indicate?
    1. Their biomass generation rate remains constant after hydration.
    2. They show decreased biomass generation 3 hours after hydration.
    3. They show high biomass generation rate during the first three hours.
    4. They have no biomass generation, even after 24 hours of hydration.
  4. How does the average replication time differ between autotrophs and heterotrophs?
    1. Heterotrophs replicated faster, with most replicating in under 10 days.
    2. Autotrophs, on average, showed longer replication times than heterotrophs.
    3. Autotrophs had a greater variation in replication time than heterotrophs.
    4. All of the above are correct.
  5. Given that most desert rains are rare and last only 1 day, what ecological role might the variation in replication times among heterotrophic and autotrophic cells play in biocrust ecosystems?
    1. It ensures that all cells contribute equally to nutrient cycling by remaining dormant
    2. It allows some bacteria to persist during environmental stresses while other are killed
    3. It reduces competition for resources between different microbial species in the biocrust
    4. It limits the overall growth of biocrusts organisms so that not many species are present

7.2. Second Figure Reading Exercise

7.2.1. Learning Objectives

Students will be able to:

  • Identify important features of the model diagram.
  • Identify the metabolic priorities during the different stages of resuscitation and hydration.
  • Predict bacterial anabolic (metabolic) activity at different times after rain events in desert ecosystems.
  • Hypothesize why microbial productivity in desert ecosystems is limited.
Experimental Background (Imminger et al., Figure 7)

Biocrusts are critical for stabilizing soils and driving nutrient cycling in arid ecosystems, making it essential to understand how these microorganisms respond to moisture.  Imminger et al. (2024) performed many experiments to test the taxonomy and metabolism of microbial communities following resuscitation after dehydration.  Using all of their results, they constructed a model which can be used to make predictions about microbial responses in biocrusts during hydration and desiccation cycles. Cyclic arid environment hydration phases are noted at the top of the figure with critical events for maintaining ecosystem functions and microbial viability noted below.  For clarification, the lower figure conceptualizes the events and timing of the main hydration phase.  Also, cyanobacteria filaments are noted as green string-like structures with many nuclei and single bacterial cells are noted by rod and cocci shapes of different colors, e.g., yellow rod with pili and circular sky blue cocci.

Fraction of anabolically active cells during hydration goes up over time, from dormant phase to the main hydration phase and finally dormancy.Figure 7: “Conceptual figure summarizing the observed resuscitation patterns of biocrust microorganisms, including metabolic processes during dry and hydration phases. Rewetting of biocrusts will stimulate microbial activity, driving major ecosystem processes (e.g., H2 oxidation, respiration, photosynthesis). Nearly all cells will become anabolically active in a rain event, but short rain phases only allow cell division in a small proportion of cells. However, even non-growing cells can use the hydration phase for repairing macromolecules and replenish reserves (such as storage compounds), which increases the chance that they persist until the next rain event.” (Imminger et al. 2024, no changes)

7.2.2. Questions

  1. What do the different-colored sphere and rod shapes in the lower diagram represent?
    1. single bacteria types
    2. cyanobacteria
    3. fungi and amoeba
    4. halophilic species
  2. Where along the lower diagram’s y-axis would you expect to find cells that are the most anabolically (metabolically) active as compared to being dormant?
    1. bottom
    2. middle
    3. top
  3. What processes occur inside cells when they are the most anabolically active, as opposed to dormant?
    1. ROS scavenging, H2 oxidation, osmoprotectant
    2. PHA degradation, ATP production, DNA repair
    3. Carbon acquisition, glycogen degradation, motility
    4. Processes that do not require water as a reactant
  4. Which process(es) occur(s) during the early hydration phase for biocrust species?
    1. DNA repair
    2. Cell division
    3. Polymer synthesis
    4. ROS scavenging
    5. ATP production
    6. Cell motility
    7. PHA degradation
  5. Based on this model, what percentage of the microbial population should be anabolically active 3 hours of the next hydration (rain) event?
    1. Approximately 70%
    2. Approximately 80%
    3. Approximately 90%
    4. All cells; 100%.
  6. Based on the metabolic priorities these researchers identified, what might be the reason microbial productivity in desert ecosystems remains limited despite the ability to rapidly activate metabolism following a rehydration event?
    1. Most microbes fail to activate metabolism within the short duration of wet periods.
    2. Metabolic activity focuses on survival and repair rather than growth and replication.
    3. Microbial communities are poorly adapted to processes that require metal cofactors .
    4. Competition among microbial and cyanobacteria species reduces available nutrients.

8. Paper Information and Licensing

8.1. Snippet paper

  • Yilmaz B, Fuhrer T, Morgenthaler D, Krupka N, Wang D, Spari D, Candinas D, Misselwitz B, Beldi G, Sauer U, Macpherson AJ. Plasticity of the adult human small intestinal stoma microbiota. Cell Host Microbe. 30(12):1773-1787. doi: 10.1016/j.chom.2022.10.002
  • The abstract and figures are unable to be copied due to restriction on the Elsevier user license: used for Elsevier open archive, which makes the final published article from certain journals free to read after an embargo period. Not able to be used for commercial or non-commercial purposes. Please see licensing information and links to the article at the journal’s web page.

8.2. Main paper

  • Imminger S, Meier DV, Schintlmeister A, Legin A, Schnecker J, Richter A, Gillor O, Eichorst SA, Woebken D. 2024. Survival and rapid resuscitation permit limited productivity in desert microbial communities. Nat Commun. 15(1):3056. doi: 10.1038/s41467-024-46920-6.
  • This article is licensed for Creative Commons use using CC BY 4.0, which allows re-use and adaptation with proper attribution and notation of any changes. See the article’s copyright information.

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Podcast Annotation and Resources in Microbiology Copyright © 2025 by Rebecca Seipelt-Thiemann; Nancy Boury; Gwendowlyn S. Knapp; Amaya Garcia Costas; and Patrick Armstrong is licensed under a Creative Commons Attribution 4.0 International License, except where otherwise noted.

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