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  1. Abstract

    Environmental parameters vary in time, and variability is inherent in soils, where microbial activity follows precipitation pulses. The expanded pulse-reserve paradigm (EPRP) contends that arid soil microorganisms have adaptively diversified in response to pulse regimes differing in frequency and duration. To test this, we incubate Chihuahuan Desert soil microbiomes under separate treatments in which 60 h of hydration was reached with pulses of different pulse duration (PD), punctuated by intervening periods of desiccation. Using 16S rRNA gene amplicon data, we measure treatment effects on microbiome net growth, growth efficiency, diversity, and species composition, tracking the fate of 370 phylotypes (23% of those detected). Consistent with predictions, microbial diversity is a direct, saturating function of PD. Increasingly larger shifts in community composition are detected with decreasing PD, as specialist phylotypes become more prominent. One in five phylotypes whose fate was tracked responds consistently to PD, some preferring short pulses (nimble responders; NIRs) and some longer pulses (torpid responders; TORs). For pulses shorter than a day, microbiome growth efficiency is an inverse function of PD, as predicted. We conclude that PD in pulsed soil environments constitutes a major driver of microbial community assembly and function, largely consistent with the EPRP predictions.

     
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    Free, publicly-accessible full text available December 1, 2025
  2. Abstract

    Soil biocrusts are characterized by the spatial self-organization of resident microbial populations at small scales. The cyanobacterium Microcoleus vaginatus, a prominent primary producer and pioneer biocrust former, relies on a mutualistic carbon (C) for nitrogen (N) exchange with its heterotrophic cyanosphere microbiome, a mutualism that may be optimized through the ability of the cyanobacterium to aggregate into bundles of trichomes. Testing both environmental populations and representative isolates, we show that the proximity of mutualistic diazotroph populations results in M. vaginatus bundle formation orchestrated through chemophobic and chemokinetic responses to gamma-aminobutyric acid (GABA) /glutamate (Glu) signals. The signaling system is characterized by: a high GABA sensitivity (nM range) and low Glu sensitivity (μM to mM), the fact that GABA and Glu are produced by the cyanobacterium as an autoinduction response to N deficiency, and by the presence of interspecific signaling by heterotrophs in response to C limitation. Further, it crucially switches from a positive to a negative feedback loop with increasing GABA concentration, thus setting maximal bundle sizes. The unprecedented use of GABA/Glu as an intra- and interspecific signal in the spatial organization of microbiomes highlights the pair as truly universal infochemicals.

     
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  3. Biological soil crusts are thin, inconspicuous communities along the soil atmosphere ecotone that, until recently, were unrecognized by ecologists and even more so by microbiologists. In its broadest meaning, the term biological soil crust (or biocrust) encompasses a variety of communities that develop on soil surfaces and are powered by photosynthetic primary producers other than higher plants: cyanobacteria, microalgae, and cryptogams like lichens and mosses. Arid land biocrusts are the most studied, but biocrusts also exist in other settings where plant development is constrained. The minimal requirement is that light impinge directly on the soil; this is impeded by the accumulation of plant litter where plants abound. Since scientists started paying attention, much has been learned about their microbial communities, their composition, ecological extent, and biogeochemical roles, about how they alter the physical behavior of soils, and even how they inform an understanding of early life on land. This has opened new avenues for ecological restoration and agriculture. Expected final online publication date for the Annual Review of Microbiology, Volume 77 is September 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates. 
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    Free, publicly-accessible full text available September 8, 2024
  4. Abstract Microbial communities are typically characterized by some degree of self-organization. In biological soil crust (biocrust) communities, vertical organization of resident populations at the mm scale is driven by organismal adaptations to physicochemical microniches. However, the extent of horizontal organization and its driving processes are unknown. Using a combination of observational and genetic mapping, we provide evidence for a highly defined, horizontal self-organization (patchiness) at the mm to cm scale in a successionally early biocrust community dominated by the pioneer cyanobacteria, Microcoleus vaginatus (Microcoleaceae) and Parifilum sp. (Coleofasciculaceae). Experiments with representative isolates of each species demonstrate that the phenomenon is driven by active spatial segregation based on cross-species sensing through the exometabolome acted upon with motility responses. Further, we show that both species share the ability to enrich for specialized cyanospheres of heterotrophic bacteria at smaller scales, and that these cyanospheres are characterized by compositional host-specificity, thus expanding the reach of spatial patchiness beyond primary producers. Our results highlight the importance of specific microbial interactions in the emergence of microbiome compositional architecture and the enhancement of microbial diversity. 
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  5. Abstract

    The pulse–reserve paradigm (PRP) is central in dryland ecology, although microorganismal traits were not explicitly considered in its inception. We asked if the PRP could be reframed to encompass organisms both large and small. We used a synthetic review of recent advances in arid land microbial ecology combined with a mathematically explicit theoretical model. Preserving the PRPs core of adaptations by reserve building, the model considers differential organismal strategies to manage these reserves. It proposes a gradient of organisms according to their reserve strategies, from nimble responders (NIRs) to torpid responders (TORs). It predicts how organismal fitness depends on pulse regimes and reserve strategies, partially explaining organismal diversification and distributions. After accounting for scaling phenomena and redefining the microscale meaning of aridity, the evidence shows that the PRP is applicable to microbes. This modified PRP represents an inclusive theoretical framework working across life-forms, although direct testing is still needed.

     
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  6. Abstract

    Diverse bacteria lead a life as pathogens or predators of other bacteria in many environments. However, their impact on emerging ecological processes in natural settings remains to be assessed. Here we describe a novel type of obligate, intracellular predatory bacterium of widespread distribution that preys on soil cyanobacteria in biocrusts. The predator,CandidatusCyanoraptor togatus, causes localized, cm-sized epidemics that are visible to the naked eye, obliterates cyanobacterial net primary productivity, and severely impacts crucial biocrust properties like nitrogen cycling, dust trapping and moisture retention. The combined effects of high localized morbidity and areal incidence result in decreases approaching 10% of biocrust productivity at the ecosystem scale. Our findings show that bacterial predation can be an important loss factor shaping not only the structure but also the function of microbial communities.

     
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  7. Stams, Alfons J. (Ed.)
    ABSTRACT Biological soil crusts (biocrusts) are communities of microbes that inhabit the surface of arid soils and provide essential services to dryland ecosystems. While resistant to extreme environmental conditions, biocrusts are susceptible to anthropogenic disturbances that can deprive ecosystems of these valuable services for decades. Until recently, culture-based efforts to produce inoculum for cyanobacterial biocrust restoration in the southwestern United States focused on producing and inoculating the most abundant primary producers and biocrust pioneers, Microcoleus vaginatus and members of the family Coleofasciculaceae (also called Microcoleus steenstrupii complex). The discovery that a unique microbial community characterized by diazotrophs, known as the cyanosphere, is intimately associated with M. vaginatus suggests a symbiotic division of labor in which nutrients are traded between phototrophs and heterotrophs. To probe the potential use of such cyanosphere members in the restoration of biocrusts, we performed coinoculations of soil substrates with cyanosphere constituents. This resulted in cyanobacterial growth that was more rapid than that seen for inoculations with the cyanobacterium alone. Additionally, we found that the mere addition of beneficial heterotrophs enhanced the formation of a cohesive biocrust without the need for additional phototrophic biomass within native soils that contain trace amounts of biocrust cyanobacteria. Our findings support the hitherto-unknown role of beneficial heterotrophic bacteria in the establishment and growth of biocrusts and allow us to make recommendations concerning biocrust restoration efforts based on the presence of remnant biocrust communities in disturbed areas. Future biocrust restoration efforts should consider cyanobacteria and their beneficial heterotrophic community as inoculants. IMPORTANCE The advancement of biocrust restoration methods for cyanobacterial biocrusts has been largely achieved through trial and error. Successes and failures could not always be traced back to particular factors. The investigation and application of foundational microbial interactions existing within biocrust communities constitute a crucial step toward informed and repeatable biocrust restoration methods. 
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  8. Abstract Background

    The determination of taxon-specific composition of microbiomes by combining high-throughput sequencing of ribosomal genes with phyloinformatic analyses has become routine in microbiology and allied sciences. Systematic biases to this approach based on the demonstrable variability of ribosomal operon copy number per genome were recognized early. The more recent realization that polyploidy is probably the norm, rather than the exception, among microbes from all domains of life, points to an even larger source bias.

    Results

    We found that the number of 16S or 18S RNA genes per cell, a combined result of the number of RNA gene loci per genome and ploidy level, follows an allometric power law of cell volume with an exponent of 2/3 across 6 orders of magnitude in small subunit copy number per cell and 9 orders of magnitude in cell size. This stands in contrast to cell DNA content, which follows a power law with an exponent of ¾.

    Conclusion

    In practical terms, that relationship allows for a single, simple correction for variations in both copy number per genome and ploidy level in ribosomal gene analyses of taxa-specific abundance. In biological terms, it points to the uniqueness of ribosomal gene content among microbial properties that scale with size.

     
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