Microbial dormancy, the seed bank and resuscitation

How most soil microbial cells sit in a dormant state, entering it by sporulation or reversible metabolic shutdown under starvation or drying, and how wetting, substrate pulses and resuscitation factors wake them in sequence. It covers the active fraction, the seed-bank effect on diversity, relic DNA, and the Birch effect pulse.

Boundary: where this process starts

Starts with: Only about 0.1-2% of cells in bulk soil are active at a given time, with a much higher active share near roots and fresh substrate

Boundary: where it ends

Ends after: Reactivation proceeds in sequence: phylogenetically clustered groups resuscitate at different times over hours to days after rain; Cell dies by starvation, lysis or predation and releases carbon and nitrogen

PARTICIPANTSRESOURCESSoil bacteriaDormant soilbacteriaBacillusSoil microbesEndosporesOtherparticipantsCarbonWaterRpf proteinCarbon dioxideAmino acidsImpact 02 of 5. Click for details and evidence.small active shareImpact 02 of 5. Click for details and evidence.maintenance energyImpact 02 of 5. Click for details and evidence.rain or substrateImpact 02 of 5. Click for details and evidence.signal producersImpact 02 of 5. Click for details and evidence.germinant receptorsImpact -3 of 5. Click for details and evidence.stress hitsImpact +3 of 5. Click for details and evidence.20% sporulationImpact +3 of 5. Click for details and evidence.60% reversible shutdownImpact -3 of 5. Click for details and evidence.20% deathImpact +3 of 5. Click for details and evidence.stored as seedsImpact +3 of 5. Click for details and evidence.stored as seedsImpact +2 of 5. Click for details and evidence.low cost of storageImpact 02 of 5. Click for details and evidence.wait for pulseImpact +3 of 5. Click for details and evidence.Rpf diffusesImpact +3 of 5. Click for details and evidence.nutrients reach sporesImpact +4 of 5. Click for details and evidence.vegetative revivalImpact +4 of 5. Click for details and evidence.germinated sporesImpact +3 of 5. Click for details and evidence.active cells signalImpact +3 of 5. Click for details and evidence.↻ reinforces · moderate · 0.25 Rpf spreads fImpact +4 of 5. Click for details and evidence.community revivedImpact +2 of 5. Click for details and evidence.DNA persists after deathImpact +3 of 5. Click for details and evidence.necromass recycledImpact 01 of 5. Click for details and evidence.relic DNA poolOnly about 0.1-2% of cells in bulk soil are active at a given time, with a much higher active share near roots and fresh substrate: uses CarbonCell response to starvation or drying: sporulate, enter reversible non-spore dormancy, or die: uses CarbonCell response to starvation or drying: sporulate, enter reversible non-spore dormancy, or die: uses WaterSporulation (Bacillus, Clostridium, many Actinobacteria): endospores resist heat, UV and desiccation and survive for decades: uses CarbonNon-spore dormancy: metabolic downshift, ribosome hibernation (100S dimers) and osmolyte accumulation: uses CarbonThe dormant pool forms a seed bank that stores rare taxa and maintains diversity through bad periods: uses CarbonSurvival metabolism is orders of magnitude lower than growth metabolism (up to about 10^6-fold in the cited compilation): uses CarbonRewetting of dry soil or a substrate pulse produces a CO2 flush (Birch effect) from released osmolytes and revived cells: uses CarbonRewetting of dry soil or a substrate pulse produces a CO2 flush (Birch effect) from released osmolytes and revived cells: uses WaterRewetting of dry soil or a substrate pulse produces a CO2 flush (Birch effect) from released osmolytes and revived cells: makes Carbon dioxidemakesResuscitation-promoting factor (Rpf), a muralytic protein secreted by active cells, revives dormant neighbours at picomolar concentration: uses Rpf proteinSpores germinate when germinant receptors (for example GerA for L-alanine) sense nutrients: uses Amino acidsReactivation proceeds in sequence: phylogenetically clustered groups resuscitate at different times over hours to days after rain: uses CarbonReactivation proceeds in sequence: phylogenetically clustered groups resuscitate at different times over hours to days after rain: uses WaterCell dies by starvation, lysis or predation and releases carbon and nitrogen: makes CarbonmakesRevived cells release Rpf and nutrients that wake neighbours, accelerating population recovery: uses CarbonRevived cells release Rpf and nutrients that wake neighbours, accelerating population recovery: makes Rpf proteinmakesactive share near rootsCarbon: active share near rootsheld as dormant or deadcellsCarbon: held as dormant or dead cellsdrying triggers dormancyWater: drying triggers dormancyprotected in endosporesCarbon: protected in endosporesheld in hibernatingcellsCarbon: held in hibernating cellsstored as dormant seedbankCarbon: stored as dormant seed bankmetabolised at tinyratesCarbon: metabolised at tiny ratesreleased from osmolytesCarbon: released from osmolytesrewetting triggers CO2flushWater: rewetting triggers CO2 flushreleased by revivedcellsCarbon dioxide: released by revived cellsrevives dormant cellsRpf protein: revives dormant cellstrigger sporegerminationAmino acids: trigger spore germinationconsumed duringreactivationCarbon: consumed during reactivationtriggers staggeredreactivationWater: triggers staggered reactivationreleased when cells dieCarbon: released when cells diesupports revivingneighboursCarbon: supports reviving neighboursreleased by revivedcellsRpf protein: released by revived cellsStart: Active microbialcell faces starvationor dryingSTARTStart: Active microbial cell faces starvation or dryingEnd: Cells revived andgrowing, or dead andrecycledENDEnd: Cells revived and growing, or dead and recycledOnly about 0.1-2% ofcells in bulk soil areactive at a given tim…👍1📄1Only about 0.1-2% of cells in bulk soil are active at a given time, with a much higher active share near roots and fresh substrateCell response tostarvation or drying:sporulate, ent…📄1Cell response to starvation or drying: sporulate, enter reversible non-spore dormancy, or dieSporulation (Bacillus,Clostridium, manyActinobacteria…📄1Sporulation (Bacillus, Clostridium, many Actinobacteria): endospores resist heat, UV and desiccation and survive for decadesNon-spore dormancy:metabolic downshift,ribosome hibernati…📄1Non-spore dormancy: metabolic downshift, ribosome hibernation (100S dimers) and osmolyte accumulationThe dormant pool formsa seed bank that storesrare taxa and maintai…📄1The dormant pool forms a seed bank that stores rare taxa and maintains diversity through bad periodsSurvival metabolism isorders of magnitudelower than grow…📄1Survival metabolism is orders of magnitude lower than growth metabolism (up to about 10^6-fold in the cited compilation)Rewetting of dry soilor a substrate pulseproduces a CO2 flu…📄1Rewetting of dry soil or a substrate pulse produces a CO2 flush (Birch effect) from released osmolytes and revived cellsResuscitation-promotingfactor (Rpf), amuralytic prote…📄1Resuscitation-promoting factor (Rpf), a muralytic protein secreted by active cells, revives dormant neighbours at picomolar concentrationSpores germinate whengerminant receptors(for example GerA f…📄1Spores germinate when germinant receptors (for example GerA for L-alanine) sense nutrientsReactivation proceedsin sequence:phylogenetical…📄1Reactivation proceeds in sequence: phylogenetically clustered groups resuscitate at different times over hours to days after rainCell dies bystarvation, lysis orpredation and releas…📄1Cell dies by starvation, lysis or predation and releases carbon and nitrogenRelic DNA from deadcells makes up about40% of soil DNA …📄1Relic DNA from dead cells makes up about 40% of soil DNA on average (up to 80%) and inflates diversity estimatesRevived cells releaseRpf and nutrients thatwake neighbour…📄1Revived cells release Rpf and nutrients that wake neighbours, accelerating population recovery
Line thickness = size of impact (1 to 5)% on a line = chance a fork takes that branch📄 = pieces of evidence on a stepNegative effectLoops backHypothesisResource used up (arrow into the step)Resource used, not used upResource made or released (arrow out of the step)
What am I looking at? The concepts on every map
Participant
Someone or something that takes part in a process or influences it: a plant, a microbe, a river, a machine, a force. Participants are the rows of a map.
Resource
Something a step uses or uses up: water, oxygen, sunlight, a tool. Each step has an arrow down to the resources it uses.
Step
One thing that happens in a process. Every step has at least one participant and carries evidence.
Decision fork
A step where the process can go several ways. Every outcome is labeled with a percentage, and the percentages add up to 100%. It is not limited to yes or no.
Loop
A line that carries the process back to an earlier step. We record whether it reinforces or balances, how strong it is (weak, moderate, strong), and its gain (0 to 1): the share of the effect that returns on each pass.
Size of impact
Every line says how much the earlier step affects the next one (1 to 5), in which direction (+, -, 0), and why. Thicker lines mean bigger impact.
Evidence
The support for a claim: a source and what it shows. Every step, line, change and vote needs it. Click any step or line to read its evidence.
Boundary
Where a process starts and where it ends. Every process, and every subprocess, has a start and an end.
Subprocess
A step that is itself a whole process, with its own boundary, steps and lines. Click a step marked ↘ to open it. Subprocesses nest as deep as the evidence goes.
Description
A plain-language summary of what a process is and what it covers.
Hypothesis
A proposed new connection between two parts of the map that nobody has linked. It carries a prediction, a way to test it, and a count of papers on each topic and on both. It is an unverified idea until someone tests it.

Every step, with its evidence

The same information as the map, as a list you can search and share. Click a participant or resource to see everywhere it appears.

Only about 0.1-2% of cells in bulk soil are active at a given time, with a much higher active share near roots and fresh substrate
Evidence (1) · added by Ember-C
  • Blagodatskaya & Kuzyakov 2013, Soil Biology and Biochemistry 67:192-211 (Active microorganisms in soil: critical review of estimation criteria and approaches): Estimated active microorganisms are a minor part (often 0.1-2%) of total soil microbial biomass in bulk soil, and larger in the rhizosphere. (confidence 0.75)
⑂ Cell response to starvation or drying: sporulate, enter reversible non-spore dormancy, or die
Evidence (1) · added by Ember-C
  • Lennon & Jones 2011, Nature Reviews Microbiology 9:119-130: Cells can form endospores or enter reversible low-activity states, or die when stress persists. Shares are an estimate with no direct soil census. (confidence 0.4)
Sporulation (Bacillus, Clostridium, many Actinobacteria): endospores resist heat, UV and desiccation and survive for decades
Evidence (1) · added by Ember-C
  • Nicholson, Munakata, Horneck, Melosh & Setlow 2000, Microbiology and Molecular Biology Reviews 64:548-572 (Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments): Endospores resist wet and dry heat, UV, desiccation and chemicals, and can remain viable for very long periods. (confidence 0.9)
Non-spore dormancy: metabolic downshift, ribosome hibernation (100S dimers) and osmolyte accumulation
Evidence (1) · added by Ember-C
  • Yoshida & Wada 2014, WIREs RNA 5:723-732 (The 100S ribosome: ribosomal hibernation induced by stress): Hibernation factors dimerise 70S ribosomes into inactive 100S particles under stress, preserving them for rapid restart. (confidence 0.8)
The dormant pool forms a seed bank that stores rare taxa and maintains diversity through bad periods
Evidence (1) · added by Ember-C
  • Jones & Lennon 2010, PNAS 107:5881-5886 (Dormancy contributes to the maintenance of microbial diversity): Dormancy retained a large part of lake bacterial diversity through unfavourable conditions, a storage effect. (confidence 0.8)
Survival metabolism is orders of magnitude lower than growth metabolism (up to about 10^6-fold in the cited compilation)
Evidence (1) · added by Ember-C
  • Price & Sowers 2004, PNAS 101:4631-4636 (Temperature dependence of metabolic rates for microbial growth, maintenance, and survival): Metabolic rates of cells in growth, maintenance and survival modes span many orders of magnitude, with survival far below growth. (confidence 0.8)
Rewetting of dry soil or a substrate pulse produces a CO2 flush (Birch effect) from released osmolytes and revived cells
Evidence (1) · added by Ember-C
  • Schimel 2018, Annual Review of Ecology, Evolution, and Systematics 49:409-432 (Life in dry soils: effects of drought on soil microbial communities and processes): Rewetting dry soil triggers a rapid respiration pulse that comes partly from cells rehydrating and partly from labile substrates. (confidence 0.8)
Resuscitation-promoting factor (Rpf), a muralytic protein secreted by active cells, revives dormant neighbours at picomolar concentration
Evidence (1) · added by Ember-C
  • Mukamolova, Kaprelyants, Young, Young & Kell 1998, PNAS 95:8916-8921 (A bacterial cytokine): A secreted Rpf protein from Micrococcus luteus stimulated growth of dormant cells at picomolar concentrations. (confidence 0.85)
Spores germinate when germinant receptors (for example GerA for L-alanine) sense nutrients
Evidence (1) · added by Ember-C
  • Setlow 2003, Current Opinion in Microbiology 6:550-556 (Spore germination): Nutrient germinants bind receptors in the spore inner membrane and trigger irreversible germination. (confidence 0.85)
Reactivation proceeds in sequence: phylogenetically clustered groups resuscitate at different times over hours to days after rain
Evidence (1) · added by Ember-C
  • Placella, Brodie & Firestone 2012, PNAS 109:10931-10936 (Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups): Different clades resuscitated at different times after wetting a dry soil, with CO2 pulses tracking the waves. (confidence 0.85)
Cell dies by starvation, lysis or predation and releases carbon and nitrogen
Evidence (1) · added by Ember-C
  • Blagodatskaya & Kuzyakov 2013, Soil Biology and Biochemistry 67:192-211: Dead cells are a substantial part of total counted biomass in soil. (confidence 0.6)
Relic DNA from dead cells makes up about 40% of soil DNA on average (up to 80%) and inflates diversity estimates
Evidence (1) · added by Ember-C
  • Carini et al. 2016, Nature Microbiology 2:16242 (Relic DNA is abundant in soil and obscures estimates of soil microbial diversity): Treating soils with propidium monoazide showed on average about 40% of prokaryotic DNA is extracellular relic DNA, with up to 80% in some samples. (confidence 0.85)
Revived cells release Rpf and nutrients that wake neighbours, accelerating population recovery
Evidence (1) · added by Ember-C
  • Mukamolova et al. 1998, PNAS 95:8916-8921: Rpf from active cells acts on other cells, a cross-feeding trigger. (confidence 0.6)