Functional succession of actively growing soil microorganisms during rewetting is shaped by precipitation history

Abstract

BackgroundRewetting of seasonally dry soils induces a burst of microbial activity and carbon mineralization that changes nutrient availability and leads to taxonomic succession. Yet the microbial functions that underpin succession are not well described. Further, how previous precipitation regimes frame microbial functional capacities after rewetting and the length of time that these effects persist remain unknown. To address these questions, we performed rewetting of seasonally dry grassland soil that experienced either mean annual or reduced precipitation during the growing season using isotopically labeled water, and sampled at five time points. We used quantitative stable isotope probing (qSIP)-informed genome-resolved metagenomics to identify actively growing bacteria and archaea, to predict their traits and analyze how these traits differ over time and between precipitation treatments.ResultsWe reconstructed 503 genomes representing bacteria and archaea from 11 phyla and 23 classes, of which 77 were from active organisms (15% of organisms). Actively growing organisms at any time point and in any treatment were primarily Actinobacteria, Alphaproteobacteria and Gammaproteobacteria. Growing organisms were significantly more abundant than non-growing organisms prior to the wet-up, suggesting that the traits that initiate succession are pre-defined at the end of the growing season or by survival over the dry season. Fast growing organisms had a relatively low number of carbohydrate active enzymes per genome compared to slower growing organisms. This suggests that although they are capable of degrading complex C sources such as plant material, they do not specialize in this process. Differential abundance of carbohydrate active enzymes in growing organisms throughout the succession implies variation in substrates over time. However, nitrogen cycling pathways differed between precipitation treatments, but in growing organisms there was no change in the abundance of genes involved over time following wetup. Comparison of gene inventories prior to wet-up revealed that many genes were significantly differentially abundant between the precipitation treatments. Surprisingly, this legacy effect waned after just one week, indicating that microbial community functions likely converge early in the growing season.ConclusionsUse of isotopic labeling of genomes of soil microorganisms during the first week after wetup revealed differences in the abundance and functional traits of actively growing organisms under two precipitation regimes. Although the legacy effect due to different rainfall inputs was short lived, it is important, given the extent of soil organic matter breakdown that occurs immediately after the first rain event in Mediterranean climates. Changes in the potential to degrade complex organic matter during the succession imply that the current paradigm that succession relies solely on labile carbon sources needs to be revisited.

A subset of viruses thrives following microbial resuscitation during rewetting of a seasonally dry California grassland soil

“…We consider vOTUs detected in viromes to be extracellularized VLPs, which are distinct from vOTUs detected in metagenomes where analysis cannot delineate between intracellular and extracellular viral populations (Supplementary Table 1). Prior to rewetting, our microbial community was dominated by Actinobacteria, Alphaproteobacteria, and Gammaproteobacteria [63]. Proteobacteria were abundant, highly active throughout wet-up, and responded early to rewetting.…”

“…Proteobacteria were abundant, highly active throughout wet-up, and responded early to rewetting. Actinobacteria also were a top-responding lineage to wet-up, but showed less overall activity despite their abundance (see Sieradzki et al, 2022 [63] for more details on the microbial and function response to rewetting).…”

“…Despite MAG and vOTU enrichment similarities, by 168 hours there is a higher degree of disordering amongst vOTUs than that of the MAGs. vOTUs most highly enriched at 24h and 48h (≥ 20 % APE) [63] in the time course appear much lower than their initial rank or are altogether undetected, and vOTUs first appearing as slightly enriched become more enriched at subsequent time points (increase in APE relative to their x-axis position) – the average change in rank from 24 hours for vOTUs is 38 and for MAGs is 9. Actinobacteria-infecting vOTUs are the most numerous active viruses across time points.…”

“…We modeled the viral contribution to microbial mortality using a range of potential burst sizes (virions per infected cell) to relate the number of approximated infectious viral particles through time to observed microbial cell death counts. Counts of microbial cell mortality were derived from our previous qSIP analysis of corresponding amplicon sequence data [63]. We used the median rate of rRNA copies lost per gram soil per day and converted this rate to per gram soil by multiplying by the number of days.…”

Propagation of viral genomes by replicating ammonia-oxidising archaea during soil nitrification

“…While one Nitrobacter MAG was obtained and both AOB and NOB viruses were also predicted, the hybrid approach developed in this study used both 12 C- and 13 C-enriched DNA to specifically target low GC mol% DNA and was tailored for the analysis of AOA populations and their viruses. A broader analysis of all viruses infecting nitrifying prokaryotic populations would therefore likely require a more comprehensive sequencing effort of all fractions throughout the CsCl gradient using quantitative SIP metagenomics [20] or alternative approaches, such as virus-targeted metagenomic viromes.…”