Response of Biological Soil Crust Diazotrophs to Season, Altered Summer Precipitation, and Year-Round Increased Temperature in an Arid Grassland of the Colorado Plateau, USA

Abstract

Biological soil crusts (biocrusts), which supply significant amounts of fixed nitrogen into terrestrial ecosystems worldwide (∼33 Tg y−1), are likely to respond to changes in temperature and precipitation associated with climate change. Using nifH gene-based surveys, we explored variation in the diazotrophic community of biocrusts of the Colorado Plateau, USA in response to season (autumn vs. spring), as well as field manipulations that increased the frequency of small volume precipitation events and year-round soil temperature. Abundance of nifH genes in biocrusts ranged from 3 × 106 to 1 × 108 g−1 soil, and nifH from heterocystous cyanobacteria closely related to Scytonema hyalinum, Spirirestis rafaelensis, and Nostoc commune comprised >98% of the total. Although there was no apparent seasonal effect on total nifH gene abundance in the biocrusts, T-RFLP analysis revealed a strong seasonal pattern in nifH composition. Spirirestis nifH abundance was estimated to oscillate 1 to >2 orders of magnitude between autumn (low) and spring (high). A year-round increase of soil temperature (2–3°C) had little effect on the diazotroph community structure over 2 years. Altered summer precipitation had little impact on diazotroph community structure over the first 1.5 years of the study, when natural background patterns across years and seasons superseded any treatment effects. However, after the second summer of treatments, nifH abundance was 2.6-fold lower in biocrusts receiving altered precipitation. Heterocystous cyanobacteria were apparently more resilient to altered precipitation than other cyanobacteria. The results demonstrate that diazotrophic community composition of biocrusts in this semi-arid grassland undergoes strong seasonal shifts and that the abundance of its dominant members decreased in response to more frequent, small volume precipitation events.

Climate change and physical disturbance cause similar community shifts in biological soil crusts

“…In addition to ambient precipitation, watering treatments consisted of frequent, 1.2 mm "rainfall events" applied by hand sprayers. Watered plots received on average 35 such events (roughly four times the average natural frequency) throughout the summer months starting in 2006 (35)(36)(37)39). Physical disturbance by human trampling started in May 1996 in ten 2 m × 5 m plots, divided as five trampled and five undisturbed controls.…”

“…Alarmingly, some experimental work suggests biocrust communities may also be highly sensitive to changing climate. Specifically, increased temperatures have been reported to reduce lichen cover in semiarid Spain (12,34), and altered precipitation patterns promoted rapid moss mortality (35) and greater variability in cyanobacterial species composition and abundance (36,37) in a cool desert of the Colorado Plateau. These changes in biocrusts due to climate manipulations also impact ecosystem processes (12,35,38).…”

Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation

“…BSC N-fixation has long been attributed to heterocystous cyanobacteria and the preponderance of cyanobacterial nifH genes observed in molecular surveys of BSCs have generally supported this hypothesis (Yeager et al, 2007(Yeager et al, , 2004(Yeager et al, , 2012. However, in this study 15 N 2 -DNA-SIP reveals that non-cyanobacterial microorganisms fix N 2 in early successional BSC samples.…”

“…Successional development of mature crust is accompanied by a change in color produced by secondary colonization with non-motile N 2 -fixing heterocystous cyanobacteria, which produce large amounts of sunscreen compounds that reduce soil albedo (Belnap, 2002;Yeager et al, 2004). These heterocystous cyanobacteria (for example, Scytonema, Spirirestis and Nostoc) increase in abundance during crust succession and are abundant in mature crusts (Yeager et al, 2007(Yeager et al, , 2012. Heterocystous cyanobacteria are numerically dominant in surveys of BSC nifH gene diversity (Yeager et al, 2007(Yeager et al, , 2004(Yeager et al, , 2012.…”

“…These heterocystous cyanobacteria (for example, Scytonema, Spirirestis and Nostoc) increase in abundance during crust succession and are abundant in mature crusts (Yeager et al, 2007(Yeager et al, , 2012. Heterocystous cyanobacteria are numerically dominant in surveys of BSC nifH gene diversity (Yeager et al, 2007(Yeager et al, , 2004(Yeager et al, , 2012. For example, 89% of 693 nifH sequences derived from Colorado Plateau and New Mexico crusts were attributed to heterocystous cyanobacteria (Yeager et al, 2007).…”