Unique Microbial Phylotypes in Namib Desert Dune and Gravel Plain Fairy Circle Soils

Abstract

Fairy circles (FCs) are barren circular patches of soil surrounded by grass species. Their origin is poorly understood. FCs feature in both the gravel plains and the dune fields of the Namib Desert. While a substantial number of hypotheses to explain the origin and/or maintenance of fairy circles have been presented, none are completely consistent with either their properties or their distribution. In this study, we investigated the hypothesis that FC formation in dunes and gravel plains is due to microbial phytopathogenesis. Surface soils from five gravel plain and five dune FCs, together with control soil samples, were analyzed using high-throughput sequencing of bacterial/archaeal (16S rRNA gene) and fungal (internal transcribed spacer [ITS] region) phylogenetic markers. Our analyses showed that gravel plain and dune FC microbial communities are phylogenetically distinct and that FC communities differ from those of adjacent vegetated soils. Furthermore, various soil physicochemical properties, particularly the pH, the Ca, P, Na, and SO 4 contents, the soil particle size, and the percentage of carbon, significantly influenced the compositions of dune and gravel plain FC microbial communities, but none were found to segregate FC and vegetated soil communities. Nevertheless, 9 bacterial, 1 archaeal, and 57 fungal phylotypes were identified as FC specific, since they were present within the gravel plain and dune FC soils only, not in the vegetated soils. Some of these FC-specific phylotypes were assigned to taxa known to harbor phytopathogenic microorganisms. This suggests that these FC-specific microbial taxa may be involved in the formation and/or maintenance of Namib Desert FCs. IMPORTANCEFairy circles (FCs) are mysterious barren circular patches of soil found within a grass matrix in the dune fields and gravel plains of the Namib Desert. Various hypotheses attempting to explain this phenomenon have been proposed. To date, however, none have been successful in fully explaining the etiology of FCs, particularly since gravel plain FCs have been largely ignored. In this study, we investigated the hypothesis that microorganisms could be involved in the FC phenomenon through phytopathogenesis. We show that the microbial communities in FC and control vegetated soil samples were significantly different. Furthermore, we detected 67 FC-specific microbial phylotypes, i.e., phylotypes present solely in both gravel plain and dune FC soils, some of which were closely related to known phytopathogens. Our results, therefore, demonstrate that microorganisms may play a role in the formation and/or maintenance of Namib Desert FCs, possibly via phytopathogenic activities. (1, 2). Common in the Namib Desert, and recently observed in the Australian outback (3), FCs are limited to arid areas that receive between 50 and 100 mm precipitation per annum. FCs are nonpermanent; they typically appear, enlarge, and disappear, with an estimated life span ranging from 22 to 60 years (4, 5).Although FCs were first reported in the 1970...

Namib Desert edaphic bacterial, fungal and archaeal communities assemble through deterministic processes but are influenced by different abiotic parameters

“…Similarly, by using T-RFLP and next generation sequencing methods, fungal communities were found to be influenced by their edaphic environment (Frossard et al 2015;Ramond et al 2014;Van der Walt et al 2016). The only study to date assessing Namib Desert archaeal communities (Van der Walt et al 2016) found that archaeal populations were significantly different in two distinct edaphic environments, namely gravel plain and dune soils.…”

“…However, all these studies focused either on a single domain (Gombeer et al 2015;Ronca et al 2015) or compared only two edaphic habitats (Frossard et al 2015;Ramond et al 2014;Van der Walt et al 2016). In this study, we have compared the archaeal, bacterial and fungal assemblages of four distinct Namib Desert soil habitats (dune, gravel plain, riverbed and saltpans), subdivided into nine soil niches.…”

“…Furthermore, as previously observed, ion concentrations had a more pronounced effect on prokaryotic (Bacterial and Archaeal) population structure than fungal populations (Sardinha et al 2003). In gravel plain soils, the higher CEC and P levels, which is indicative of more fertile soil (Davatgar et al 2012), might explain the highly diverse bacterial, archaeal and fungal assemblages observed, as the higher abundance of resources could support a more diverse community of The ubiquitous presence of bacteria in all nine soil niches was not surprising, as bacteria are well adapted to survive in extreme edaphic environments, and have consistently been detected across all Namib Desert edaphic environments (Gombeer et al 2015;Makhalanyane et al 2013;Prestel et al 2008;Ramond et al 2014;Ronca et al 2015;Stomeo et al 2013;Valverde et al 2015;Van der Walt et al 2016).The absence of Archaea and Fungi from dune top and dune slope soils could reflect the highly unstable nature of the soil in this environment, which has a high dispersal rate of soil particles (Livingstone 2013). However, the possibility that the limitations of techniques used in this study resulted in the absence of Archaeal and Fungal OTUs should not be eliminated, as T-RFLP analysis is only able to detect the most abundant phylotypes present (Nocker et al 2007).…”

“…In the Namib Desert, we have conclusively demonstrated that niche partitioning/selection is a critical process involved in the assembly of the bacterial fraction of edaphic and hypolithic microbial communities (Gombeer et al 2015;Makhalanyane et al 2013;Ramond et al 2014;Ronca et al 2015). Most similar research has focussed on the Domain Bacteria, with few multi-domain studies which include Fungi (Ramond et al 2014), protists (Valverde et al 2015), viruses (Prestel et al 2008), and/or Archaea (Van der Walt et al 2016). Since Bacteria, Fungi and Archaea are involved in distinct functional aspects of ecosystem processes and biogeochemical cycling (e.g.…”

Contrasting Global Patterns of Spatially Periodic Fairy Circles and Regular Insect Nests in Drylands

“…The origin of these FCs in water-limited drylands has puzzled scientists for decades (Sahagian, 2017;van Rooyen et al, 2004). The hypotheses include (a) allelopathic influences of a plant that no longer occurs in FCs (Meyer et al, 2015;Theron, 1979); (b) seepage of carbon monoxide, hydrocarbons, or other volatiles from below ground that kills grass in regular patterns (Albrecht et al, 2001;Jankowitz et al, 2008;Naude et al, 2011); (c) an unspecified microbial effect (Eicker et al, 1982;Ramond et al, 2014;van der Walt et al, 2016); (d) faunal removal of grasses by termites (Becker & Getzin, 2000;Juergens, 2013;Moll, 1994;Vlieghe et al, 2015) or detrimental influence on grasses by ants (Picker et al, 2012); and (e) self-organized emergent vegetation patterning arising from competitive and facilitative interactions between grasses (Cramer et al, 2017;Cramer & Barger, 2013;Getzin et al, 2015aGetzin et al, , 2015bGetzin et al, , 2016Ravi et al, 2017;Tschinkel, 2012;van Rooyen et al, 2004).…”