Biocrust cyanobacteria are susceptible to bacterial predation

Cyanobacteria found within biocrusts are pivotal to the development and health of these dryland microbial communities. Discovery of a biocrust-native predatory bacterium of cyanobacteria indicates there are internal and unknown disease factors these communities must contend with.
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Predatory bacteria, heterotrophs that rely on other living bacteria for nutrients and replication, are a widespread phenomenon in a multitude of environments1 but were undocumented in biological soil crusts (biocrusts). Biocrusts are soil surface microbial communities that are ubiquitous in drylands, providing important services including soil stabilization2,3 and nutrient addition, contributing fixed C and N4 in otherwise nutrient-deficient soils. Key to the establishment of biocrusts are cyanobacteria, with their ability to stabilize uncolonized soil, providing an environment for the further establishment of a range of microbes. Recognized threats to these communities are primarily anthropogenic; however, in our recent article we were able to document the presence, and functional impact of a predatory bacterium, Candidatus Cyanoraptor togatus, native to biocrusts that preys specifically upon cyanobacteria species that are foundational members of biocrusts.

Using infected biocrusts5 identified via “plaques” or circular clearings within healthy biocrusts, we enriched for and described a new predatory bacterium, the first known in biocrusts, and provide evidence for the devastating impact of bacterial predation on biocrust function. Genomic studies of Cyanoraptor revealed that it has no close relation to other predatory bacteria, and taxonomic classification was only possible at the family level, indicating that Cyanoraptor was an entirely new genus. Imaging of Cyanoraptor’s infection progression allowed us to not only visualize its unique infrastructure containing double membranes resulting in compartmentalization but also document its complex life cycle, providing clues to its mode of infection. Much like the most widely studied predatory bacterium, Bdellovibrio bacteriovorus, infection includes a dual strategy containing attack and replication phases6. During attack Cyanoraptor docks with its prey before penetrating its host and lodging within the host’s cytoplasm, beginning the replication phase and growing into pseudo-filaments before dividing into individual progeny which are released into the environment, returning to their attack phase. Its life cycle combined with its lack of genes for all but two amino acid biosynthesis pathways and absence of motility or chemotaxis genes indicates it is totally reliant upon its host for reproduction and transmission.

Cyanoraptor’s preferred meal, Microcoleus vaginatus is arguably the most widespread terrestrial cyanobacterium which suggests Cyanoraptor’s impact may be likewise widespread. A meta-analysis seems to confirm this result, with detection of Cyanoraptor or similar organisms found in all but one location surveyed and these surveys were likely an underestimate as they were simply of biocrusts, not those with signs of infection. The presence of similar organisms suggests that there are other unidentified predators within biocrusts; however, further research tracking plaques globally will be necessary to confirm this.

Spotting plaques is relatively simple but requires dedication; they are quite evident but only after rain events when biocrusts “green-up” as cyanobacteria move to the surface. This required that we invariably checked weather forecasts at multiple locations, driving hundreds of miles as soon as storms were reported in order to catch active and infected biocrusts. Using these field samples, we compared a battery of key functions of biocrusts within and outside plaques that speak to bacterial predation’s ability to decimate biocrusts’ important environmental contributions. Likely due to the reduction in cyanobacteria there were severe losses in primary production, robbing soils of important C inputs. This combined with shifts between organic and inorganic N robs soils of necessary nutrients. Decreases in photoprotective pigments suggested a reduction in secondary colonizing cyanobacteria, which could be indicative of the hindrance of natural biocrust succession, further reducing its beneficial environmental contributions. Cyanobacteria also exude copious amounts of exopolysaccharides, but predation resulted in significant decline within plaques, potentially responsible for declines we documented in moisture retention that consequently decreased dust trapping ability. Bacterial predation’s obliteration of these ecologically important services will severely reduce the primary benefits biocrusts provide.

Implications for biocrust health

Biocrusts are already under assault from increased anthropogenic factors such as trampling7 and livestock grazing8. While predatory bacteria may be a native component of the biocrust community, discovery of Cyanoraptor and like organisms only furthers concern for the stability of these communities. Projected increases in temperature and reduced rainfall are likely to cause biocrusts to revert to early successional stages that are primarily composed of cyanobacteria. As a greater portion of biocrusts shift to cyanobacterial dominant communities these predators will be increasingly destructive. With the likelihood that there are other predatory bacteria of biocrust cyanobacteria, identification of further organisms, their mode of action and functional impacts are necessary to appropriately estimate their worldwide contributions and the current and future fate in the face of climate change.

Implications for restoration

Outside threats to biocrust health have resulted in a wealth of research on restoration methods; however, our discovery suggests we need to reevaluate these methods. Commonly, damaged biocrusts are harvested and used for production of greater quantities of biomass before application to field locations providing ample opportunity for these predators to establish in areas that are already disadvantaged; in fact, our previous work5 demonstrated mass mortality of cyanobacteria within restoration inoculum rendering it unfit for field application. However, relatively simple measures can be taken to remediate predatory bacterial impact by collecting biocrusts after rain events and avoiding plaques; additionally, inoculum can be monitored for infection while in production. However, we recognize that these strategies limit field collection and make production more labor intensive.

References

  1. Jurkevitch, E. & Mitchell, R. Preface. in The Ecology of Predation at the Microscale (eds. Jurkevitch, E. & Mitchell, R.) vii–viii (Springer Nature Switzerland, 2020).
  2. Belnap, J. & Gardner, J. Soil microstructure in soils of the Colorado Plateau: The role of the cyanobacterium Microcoleus vaginatus. West. North Am. Nat. 53, 40–47 (1993).
  3. Garcia-Pichel, F. & Wojciechowski, M. F. The evolution of a capacity to build supra-cellular ropes enabled filamentous cyanobacteria to colonize highly erodible substrates. PLoS One 4, 4–9 (2009).
  4. Elbert, W. et al. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat. Geosci. 5, 459–462 (2012).
  5. Bethany, J., Giraldo-Silva, A., Nelson, C., Barger, N. N. & Garcia-Pichel, F. Optimizing production of nursery-based biological soil crusts for restoration of arid land soils. Appl. Environ. Microbiol. AEM.00735-19 (2019) doi:10.1128/AEM.00735-19.
  6. Jurkevitch, E. & Davidov, Y. Phylogenetic Diversity and Evolution of Predatory Prokaryotes. in Predatory Prokaryotes - Biology, Ecology and Evolution (ed. Jurkevitch, E.) 11–56 (Springer Berlin Heidelberg, 2007). doi:10.1007/7171_052.
  7. Cole, D. N. Trampling disturbance and recovery of cryptogamic soil crusts in Grand-Canyon-National-Park. Gt. Basin Nat. 50, 321–325 (1990).
  8. Daryanto, S., Eldridge, D. J. & Wang, L. Ploughing and grazing alter the spatial patterning of surface soils in a shrub-encroached woodland. Geoderma 200201, 67–76 (2013).

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