skip to main content

Title: High impact of bacterial predation on cyanobacteria in soil biocrusts

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.

more » « less
Award ID(s):
2025166 2129537
Author(s) / Creator(s):
; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Communications
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Drylands are a widely degraded biome characterized by low productivity and high abiotic stress. Biological soil crust (biocrust) inoculants hold promise as a rehabilitation material in drylands, useful for boosting ecosystem functions including stabilization of eroding soil surfaces. However, biocrust materials cultivated ex situ by humans inconsistently establish under field conditions. We tested two approaches aimed at improving field establishment of biocrust inoculum: exposing the organisms within the inoculum to abiotic stress in an attempt to harden them, and applying habitat ameliorations intended to reduce the stressfulness of the environment. We hypothesized that both approaches in concert would lead to the most consistent field establishment of biocrusts. Overall, addition of biocrust inoculum did enhance biocrust establishment over the 1.5‐year duration of the study but did not result in full recovery. Generally, hardened biocrust inoculum performed no better than inoculum that was not hardened, although one indicator (chlorophylla) was enhanced by addition of hardened inoculum in some circumstances. Temporary irrigation was initially an effective habitat amelioration but had no effect on biocrust establishment by 1.5 years. In contrast, application of jute net to the soil surface promoted biocrust establishment both in synergy with and in the absence of inoculum addition. We hypothesize that jute net stabilizes the soil surface, reduces abiotic stress, and enhances resource availability, overcoming barriers to establishment of biocrusts. Currently, there is broad support for the efficacy of habitat amelioration approaches in biocrust rehabilitation, but effective hardening techniques remain elusive.

    more » « less
  2. Abstract

    The size and frequency of resource pulses can affect plant interactions and increase the abundance of invasive species relative to native species. We examined resource pulses generated during the desiccation and rehydration of communities of native biological soil crust (biocrust)‐forming mosses, in the context of positive associations between biocrusts and the invasive forb,Centaurea stoebe.

    We surveyedCentaureaand biocrust cover and evaluated how interactions amongCentaurea, biocrusts and water pulses influenced plant biomass and soil nitrogen in a field experiment.Centaureaseedling and biocrust interactions were also compared in a greenhouse experiment to evaluate differences related to life stage.

    In field surveys,Centaureaand biocrusts were positively associated. Across water pulse treatments, biocrust biomass decreased whenCentaureawas removed, indicating thatCentaureafacilitated biocrusts. Biocrusts did not affect adultCentaureain the field, butCentaureaseedling biomass was greater when grown with biocrusts in the greenhouse. Water pulses did not affect plant biomass, but interactions betweenCentaureaand biocrusts corresponded with variation in the effect of water pulses on soil nitrogen which were not evident whenCentaureaor biocrusts were grown alone. Twenty‐four hours after large water pulses were added, soilwas nine times higher in plots where biocrusts andCentaureaco‐occurred compared with small water pulse plots. In these same plots, soiltended to be lower at the end of the experiment.

    These results highlight positive interactions between an invasive exotic forb and native moss biocrust. Water pulses influenced soil nitrogen availability when both plants co‐occurred, but did not affect plant biomass, suggesting that resource pulses and species interactions can interact to affect ecosystem processes.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

    more » « less
  3. Abstract

    Understanding the importance of biotic interactions in driving the distribution and abundance of species is a central goal of plant ecology. Early vascular plants likely colonized land occupied by biocrusts — photoautotrophic, surface‐dwelling soil communities comprised of cyanobacteria, bryophytes, lichens and fungi — suggesting biotic interactions between biocrusts and plants have been at play for some 2,000 million years. Today, biocrusts coexist with plants in dryland ecosystems worldwide, and have been shown to both facilitate or inhibit plant species performance depending on ecological context. Yet, the factors that drive the direction and magnitude of these effects remain largely unknown.

    We conducted a meta‐analysis of plant responses to biocrusts using a global dataset encompassing 1,004 studies from six continents.

    Meta‐analysis revealed there is no simple positive or negative effect of biocrusts on plants. Rather, plant responses differ by biocrust composition and plant species traits and vary across plant ontogeny. Moss‐dominated biocrusts facilitated, while lichen‐dominated biocrusts inhibited overall plant performance. Plant responses also varied among plant functional groups: C4grasses received greater benefits from biocrusts compared to C3grasses, and plants without N‐fixing symbionts responded more positively to biocrusts than plants with N‐fixing symbionts. Biocrusts decreased germination but facilitated growth of non‐native plant species.

    Synthesis. Results suggest that interspecific variation in plant responses to biocrusts, contingent on biocrust type, plant traits, and ontogeny can have strong impacts on plant species performance. These findings have important implications for understanding biocrust contributions to plant productivity and community assembly processes in ecosystems worldwide.

    more » « less
  4. 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. 
    more » « less
  5. Climate change is expanding drylands even as land use practices degrade them. Representing ∼40% of Earth’s terrestrial surface, drylands rely on biological soil crusts (biocrusts) for key ecosystem functions including soil stability, biogeochemical cycling, and water capture. Understanding how biocrusts adapt to climate change is critical to understanding how dryland ecosystems will function with altered climate. We investigated the sensitivity of biocrusts to experimentally imposed novel climates to track changes in productivity and stability under both warming and cooling scenarios. We established three common gardens along an elevational-climate gradient on the Colorado Plateau. Mature biocrusts were collected from each site and reciprocally transplanted intact. Over 20 months we monitored visible species composition and cover, chlorophyll a, and the composition of soil bacterial communities using high throughput sequencing. We hypothesized that biocrusts replanted at their home site would show local preference, and biocrusts transplanted to novel environments would maintain higher cover and stability at elevations higher than their origin, compared to at elevations lower than their origin. We expected responses of the visible biocrust cover and soil bacterial components of the biocrust community to be coupled, with later successional taxa showing higher sensitivity to novel environments. Only high elevation sourced biocrusts maintained higher biocrust cover and community stability at their site of origin. Biocrusts from all sources had higher cover and stability in the high elevation garden. Later successional taxa decreased cover in low elevation gardens, suggesting successional reversal with warming. Visible community composition was influenced by both source and transplant environment. In contrast, soil bacterial community composition was not influenced by transplant environments but retained fidelity to the source. Thus, responses of the visible and soil bacterial components of the biocrust community were not coupled. Synthesis: Our results suggest biocrust communities are sensitive to climate change, and loss of species and function can be expected, while associated soil bacteria may be buffered against rapid change. 
    more » « less