Land degradation effects on composition of pioneering soil communities: An alternative successional sequence for dryland cyanobacterial biocrusts

Abstract

In drylands, soil surfaces in interplant spaces are usually covered by biocrusts, which consist of communities of heterotrophic and chemoautotrophic bacteria, cyanobacteria, mosses, lichens, microalgae, fungi and other organisms. Cyanobacteria are of special interest because of their capacity to promote biocrust succession or increase soil fertility and stability. Therefore, some studies have analyzed their communities in different ecosystems, focusing on how different factors, such as temperature or altitude, influence their composition. Nevertheless, to our knowledge, the relationship between ecosystem degradation and cyanobacterial community composition has not yet been studied in depth. This could be determinant for the successful development of tools for restoring degraded biocrusts by cyanobacterial inoculation. Thus, the objective of this study was to analyze the effect of the ecosystem degradation level on cyanobacteria composition from topsoil communities, where they are keystone pioneering organisms. To do this, we analyzed the cyanobacterial diversity by molecular sequencing (16S rRNA gene) of the DNA extracted from biocrusts at different developmental stages, which were collected from three ecosystems in southeastern Spain. The selected ecosystems represent different "land-condition" states as a result of degradation processes. In one of them soil was removed by mining (the Gador quarry), the second is a natural badland area (El Cautivo) where water erosion is intense, and the third ecosystem is a well-preserved area (Balsa Blanca). Our findings show that cyanobacterial richness decreases (up to 28 OTUs) as degradation increases and biocrust developmental stage decreases. Also, the relative abundances of most of the species were significantly correlated with the degradation state of the sampling site, either showing a positive or negative trend. Two of the species which increased in abundance with site degradation, and were especially abundant in incipient biocrusts, were Leptolyngbya frigida and Trichocoleus desertorum, while other species, also showing an increase in abundance with degradation, but having a higher relative abundance in most developed biocrusts, were Nostoc commune, Tolypothrix distorta and Scytonema sp. The significant correlation of these species with degradation at different biocrusts developmental stages, suggests an alternative developmental sequence for drylands, at least in more degraded ecosystems. In less degraded ones, the composition of the major cyanobacterial groups followed the common pattern of bundle-forming cyanobacteria (54.7%) pertaining to the Microcoleus genus followed by other non-heterocystous filamentous (17.4%), unicellular/colonial (7.5%) and heterocystous cyanobacteria (1.1%). In comparison, the cyanobacterial groups dominating the most incipient biocrusts, colonizing the most degraded soil, were the filamentous non-heterocystous (50.7%) and the bundleforming cyanobacteria (48.9%). Therefore, our results show that some cyanobacterial species, which do not belong to traditional pioneer genera, are frequent colonizers of degraded soils, and then, they could be potentially used for producing a more efficient inoculum for inducing biocrust formation and restoring degraded soils. Finally, it is also remarkable that L. frigida appears as dominant in some biocrusts from drylands (up to 74.9% of abundance) being therefore demonstrated its wide distribution in nonpolar biomes and its capacity to also inhabit degraded arid soils ; This work was supported by the projects RESUCI (CGL 2014-59946-R), the project REBIOARID (RTI 2018-101921-B-I00), and the GL 2013-44870-R and GL 2017-6258-R projects, all of them founded by the Spanish National Plan for Research and the European Union ERDF funds