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Abstract Future climates will alter the frequency and size of rain events in drylands, potentially affecting soil microbes that generate carbon feedbacks to climate, but field tests are rare. Topsoils in drylands are commonly colonized by biological soil crusts (biocrusts), photosynthesis‐based communities that provide services ranging from soil fertilization to stabilization against erosion. We quantified responses of biocrust microbial communities to 12 years of altered rainfall regimes, with 60 mm of additional rain per year delivered either as small (5 mm) weekly rains or large (20 mm) monthly rains during the summer monsoon season. Rain addition promoted microbial diversity, suppressed the dominant cyanobacterium,Microcoleus vaginatus, and enhanced nitrogen‐fixing taxa, but did not consistently increase microbial biomass. The addition of many small rain events increased microbial biomass, whereas few, large events did not. These results alter the physiological paradigm that biocrusts are most limited by the amount of rainfall and instead predict that regimes enriched in small rain events will boost cyanobacterial biocrusts and enhance their beneficial services to drylands.
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Urea-based mutualistic transfer of nitrogen in biological soil crusts
Abstract Foundational to the establishment and recovery of biocrusts is a mutualistic exchange of carbon for nitrogen between pioneer cyanobacteria, including the widespread Microcoleus vaginatus, and heterotrophic diazotrophs in its cyanosphere. In other such mutualisms, nitrogen is transferred as amino acids or ammonium, preventing losses through specialized structures, cell apposition or intracellularity. Yet, in the biocrust symbiosis relative proximity achieved through chemotaxis optimizes the exchange. We posited that further partner specificity may stem from using an unusual nitrogen vehicle, urea. We show that representative mutualist M. vaginatus PCC 9802 possesses genes for urea uptake, two ureolytic systems, and the urea cycle, overexpressing only uptake and the rare urea carboxylase/allophanate hydrolase (uc/ah) when in co-culture with mutualist Massilia sp. METH4. In turn, it overexpresses urea biosynthesis, but neither urease nor urea uptake when in co-culture. On nitrogen-free medium, three cyanosphere isolates release urea in co-culture with M. vaginatus but not in monoculture. Conversely, M. vaginatus PCC 9802 grows on urea down to the low micromolar range. In natural biocrusts, urea is at low and stable concentrations that do not support the growth of most local bacteria, but aggregates of mutualists constitute dynamic microscale urea hotspots, and the cyanobacterium responds chemotactically to urea. The coordinated gene co-regulation, physiology of cultured mutualists, distribution of urea pools in nature, and responses of native microbial populations, all suggest that low-concentration urea is likely the main vehicle for interspecies N transfer, helping attain partner specificity, for which the rare high-affinity uc/ah system of Microcoleus vaginatus is likely central.
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- Award ID(s):
- 2129537
- PAR ID:
- 10572920
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 19
- Issue:
- 1
- ISSN:
- 1751-7362
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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