Abstract
Microbes in hot desert soil partake in core ecosystem processes e.g., biogeochemical cycling of carbon. Nevertheless, there is still a fundamental lack of insights regarding short-term (i.e., over a 24-hour [diel] cycle) microbial responses to highly fluctuating microenvironmental parameters like temperature and humidity. To address this, we employed T-RFLP fingerprinting and 454 pyrosequencing of 16S rRNA-derived cDNA to characterize potentially active bacteria in Namib Desert soil over multiple diel cycles. Strikingly, we found that significant shifts in active bacterial groups could occur over a single 24-hour period. For instance, members of the predominant Actinobacteria phyla exhibited a significant reduction in relative activity from morning to night, whereas many Proteobacterial groups displayed an opposite trend. Contrary to our leading hypothesis, environmental parameters could only account for 10.5% of the recorded total variation. Potential biotic associations shown through co-occurrence networks indicated that non-random inter- and intra-phyla associations were ‘time-of-day-dependent’ which may constitute a key feature of this system. Notably, many cyanobacterial groups were positioned outside and/or between highly interconnected bacterial associations (modules); possibly acting as inter-module ‘hubs’ orchestrating interactions between important functional consortia. Overall, these results provide empirical evidence that bacterial communities in hot desert soils exhibit complex and diel-dependent inter-community associations.
Highlights
Macro- and micro-environmental parameters are critical in governing community assembly and function[1,2]
Well-characterized circadian rhythms facilitate adaptive strategies within these habitats that include the reproductive behaviour of desert locusts[54], heterothermy in desert mammals[55] and in desert plant physiology[56]
It has been reported that the globally distributed circadian gene locus, cpmA, is highly conserved in key microbial phylotypes such as Cyanobacteria[57], which suggests a key role in the maintenance of intracellular homeostasis and adaptation[58]
Summary
The light-dark (diel) cycle drives behavioral responses that are an essential component of life in hot desert systems. Light-dependent changes in microbial gene expression are a feature in hot desert biological soil crusts[23]. In situ soil relative humidity (RH) levels were highly variable over each diel cycle (Fig. 1; time-points; P < 0.001). Significant differences were found between days for nitrate (F4.45 = 3.54, P = 0.017) and magnesium (F4.45 = 3.01, P = 0.037) but this was likely to be a consequence of spatial heterogeneity, with a nutrient ‘hotspot’ recorded for a single biological replicate sampled on day 2 (Fig. S1). Changes in active bacterial communities revealed by T-RFLP analysis. Community fingerprinting by T-RFLP rRNA gene (cDNA) analysis recorded a total of 27 unique terminal restriction fragments (TRFs), likely representing the most active bacterial taxa present in this soil system[59]. Significant shifts in potentially active bacterial communities was recorded between time-points was confirmed by PERMANOVA (F4,45 = 5.51, P = 0.007). ACE 253(110) 556(292) 609(298) 251(173) 278(164) 299(189) 923(299) 234(48) 297(76) 492(92) 561(248) 180(109) 167(81) 422(189) 325(98)
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