Received: 17 November 2017 | Accepted: 15 January 2018 DOI: 10.1111/gcb.14113 PRIMARY RESEARCH ARTICLE Drought consistently alters the composition of soil fungal and bacterial communities in grasslands from two continents Raul Ochoa-Hueso1 | Scott L. Collins2 | Manuel Delgado-Baquerizo3 | Kelly Hamonts4 | William T. Pockman2 | Robert L. Sinsabaugh2 | Melinda D. Smith5 | Alan K. Knapp5 | Sally A. Power4 1Department of Ecology, Autonomous University of Madrid, Madrid, Spain Abstract 2Department of Biology, University of New The effects of short-term drought on soil microbial communities remain largely Mexico, Albuquerque, NM, USA unexplored, particularly at large scales and under field conditions. We used seven 3Cooperative Institute for Research in Environmental Sciences, University of experimental sites from two continents (North America and Australia) to evaluate Colorado, Boulder, CO, USA the impacts of imposed extreme drought on the abundance, community composi- 4 Hawkesbury Institute for the Environment, tion, richness, and function of soil bacterial and fungal communities. The sites Western Sydney University, Penrith, New South Wales, Australia encompassed different grassland ecosystems spanning a wide range of climatic and 5Department of Biology and Graduate soil properties. Drought significantly altered the community composition of soil bac- Degree Program in Ecology, Colorado State University, Fort Collins, CO, USA teria and, to a lesser extent, fungi in grasslands from two continents. The magnitude of the fungal community change was directly proportional to the precipitation gradi- Correspondence Raul Ochoa-Hueso, Department of Ecology, ent. This greater fungal sensitivity to drought at more mesic sites contrasts with the Autonomous University of Madrid, Madrid, generally observed pattern of greater drought sensitivity of plant communities in Spain. Email: [email protected] more arid grasslands, suggesting that plant and microbial communities may respond differently along precipitation gradients. Actinobateria, and Chloroflexi, bacterial Funding information Western Sydney University; Hermon Slade phyla typically dominant in dry environments, increased their relative abundance in Foundation, Grant/Award Number: response to drought, whereas Glomeromycetes, a fungal class regarded as widely P00021516; NSF Macrosystems Biology, Grant/Award Number: EF-1137378, symbiotic, decreased in relative abundance. The response of Chlamydiae and Teneri- EF-1137363, EF-1137342, EF-1137293 cutes, two phyla of mostly pathogenic species, decreased and increased along the precipitation gradient, respectively. Soil enzyme activity consistently increased under drought, a response that was attributed to drought-induced changes in microbial community structure rather than to changes in abundance and diversity. Our results provide evidence that drought has a widespread effect on the assembly of microbial communities, one of the major drivers of soil function in terrestrial ecosystems. Such responses may have important implications for the provision of key ecosystem services, including nutrient cycling, and may result in the weakening of plant–micro- bial interactions and a greater incidence of certain soil-borne diseases. KEYWORDS drought, enzyme activities, microbial community, rainfall manipulation, soil-borne pathogens 2818 | © 2018 John Wiley & Sons Ltd wileyonlinelibrary.com/journal/gcb Glob Change Biol. 2018;24:2818–2827. OCHOA-HUESO ET AL. | 2819 1 | INTRODUCTION and, therefore, understanding how microbial community structure and functioning in grasslands respond to drought is essential for pre- Microorganisms play fundamental roles as primary producers and dicting impacts of climate change on the global C cycle. Climate decomposers and provide important ecosystem services such as models for the Central and Southwest US, where grasslands domi- organic matter decomposition and nutrient cycling and storage nate the landscape, predict an intensification of the hydrological (Bardgett & van der Putten, 2014; van der Heijden, Bardgett, & van cycle, with high interannual precipitation variability and fewer but Straalen, 2008). The structure and activity of microbial communities larger rain events (Cook et al., 2015). Similarly, for south-eastern in soils is influenced by substrate properties, particularly soil pH and Australia, where land conversion has transformed more than 90% of organic matter content, and vegetation type (Delgado-Baquerizo native woodlands into seminatural grasslands, the most recent cli- et al., 2016a; Fierer & Jackson, 2006); at larger spatial and temporal mate models predict an increase in the occurrence of extreme pre- scales long-term climatic phenomena such as increasing aridity have cipitation events interspersed with longer droughts and shifts in also been associated with lower bacterial and fungal abundance and precipitation seasonality but little change in total precipitation lower microbial diversity (Maestre et al., 2015). However, much less (McLaughlin, 2014). is known about how short-term climatic processes, including the In this study, we evaluated the impacts of comparable extreme more extreme drought events forecast (Cook, Ault, & Smerdon, drought simulation experiments (50% precipitation reduction) con- 2015), will affect microbial communities and the ecosystem services ducted at seven grasslands located in two continents, North America they mediate. and Australia (Table 1; Figure 1). We sampled each site during the Climate models forecast widespread changes in precipitation 2nd or 3rd year of imposed drought and measured (i) soil microbial regimes, including longer, more intense droughts (McLaughlin, 2014), community richness (number of phylotypes) and composition (rela- causing desertification and promoting the expansion of drylands tive abundance of phylotypes), (ii) microbial abundance, and (iii) the globally (Huang, Yu, Guan, Wang, & Guo, 2016). Field-based climate potential activities of enzymes associated with decomposition and change studies have traditionally focused on aboveground responses nutrient cycling by soil microbial communities. The consistency of (e.g., plant productivity, biomass, and community composition) of treatment types between sites in the USA (66% precipitation reduc- local studies, whereas belowground responses, particularly those of tion during the growing season, equivalent to an annual reduction of microbial communities, have received much less attention (Wilcox, 50%) and Australia (50% year-round reduction; Power et al., 2016) von Fischer, Muscha, Petersen, & Knapp, 2015; Wilcox et al., 2017). allows for evaluation of responses to experimental drought across Experimental approaches across multiple sites and continents, where continents. We hypothesized that, at both intercontinental and local contrasting climatic and edaphic conditions may mediate the impacts scales, experimental drought will significantly alter the assembly of of changing precipitation regimes, are equally needed to accurately microbial communities in grasslands, with bacterial communities predict the response of microbial communities to extreme drought being more sensitive than fungi to water limitation (Austin et al., (Fridley, Grime, Askew, Moser, & Stevens, 2011; Grime et al., 2008). 2004; Clark, Campbell, Grizzle, Acosta-Martınez, & Zak, 2009). Drought experiments and meta-analyses consistently predict nega- Specifically, we predicted that the relative abundance of bacterial tive impacts of drought on the diversity and abundance of soil microbial communities (Wu, Dijkstra, Koch, Penuelas,~ & Hungate, TABLE 1 Environmental characteristics of study sites 2011), with bacteria typically considered more sensitive than fungi Grassland MAP MAT (Evans & Wallenstein, 2012; Fry et al., 2016). Given the strong link Site name Code type (mm) (°C) pH between microbial communities and soil functioning, any alteration Sevilleta National SEV Desert 242 13.3 8.5 in the composition of microbial communities due to climate change Wildlife Refuge Black might disrupt the functioning of soil, and thus the supply of ecosys- Sevilleta National SEV Shortgrass 242 13.3 8.8 tem services (Bellard, Bertelsmeier, Leadley, Thuiller, & Courchamp, Wildlife Refuge Blue 2012; McLaughlin, 2014). Because of this, improving our under- Central Plains SGS Shortgrass 342 8.6 6.2 standing of the role of altered precipitation regimes in the regulation Experimental Range of soil microbial communities is of paramount importance to accu- High Plains WYO Mixed 384 7.6 7.1 rately predict changes in terrestrial ecosystem processes linked to Grasslands Research future climate change scenarios (Delgado-Baquerizo et al., 2016b; Center Maestre et al., 2015). Hays Agricultural HAYS Mixed 577 12.0 7.2 Research Center Grasslands are critically important components of terrestrial ecosystem feedbacks to climate change. They represent ca. 40% of Konza Prairie KNZ Tallgrass 860 12.9 6.4 Biological Station the total land surface, store ca. 3.4 t C haÀ1 yearÀ1 and provide DRI-Grass DG Australian 800 17.0 6.6 multiple ecosystem services (McLaughlin, 2014). Grasslands also Experimental Site grassland greatly contribute to regulate the interannual variability in the soil C sink at the global scale (Ahlstrom€ et al., 2015; Poulter et al., 2014) MAP, mean annual precipitation; MAT, mean annual temperature. 2820 | OCHOA-HUESO ET AL. (a) (b) EDGE WYO SGS 1,600 HAYS KNZ 1,400 1,200 1,000 800 EDGE Latitude 600 SEV 400 200 30 32 34 36 38 40 42 44 –110 –105 –100