Responses of soil bacterial and fungal communities to extreme desiccation and rewetting

The ISME Journal (2013) 7, 2229–2241 & 2013 International Society for Microbial Ecology All rights reserved 1751-7362/13 www.nature.com/ismej ORIGINAL ARTICLE Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Romain L Barnard1,2,4,5, Catherine A Osborne1,3,5 and Mary K Firestone1 1 Department of Environmental Science, Policy and Management, University of California, Berkeley CA, USA; Institute of Agricultural Sciences, ETH Zurich, Zurich, Switzerland and 3Monash University, Clayton, Victoria, Australia 2 The microbial response to summer desiccation reflects adaptation strategies, setting the stage for a large rainfall-induced soil CO2 pulse upon rewetting, an important component of the ecosystem carbon budget. In three California annual grasslands, the present (DNA-based) and potentially active (RNA-based) soil bacterial and fungal communities were tracked over a summer season and in response to controlled rewetting of intact soil cores. Phylogenetic marker genes for bacterial (16S) and fungal (28S) RNA and DNA were sequenced, and the abundances of these genes and transcripts were measured. Although bacterial community composition differed among sites, all sites shared a similar response pattern of the present and potentially active bacterial community to dry-down and wet-up. In contrast, the fungal community was not detectably different among sites, and was largely unaffected by dry-down, showing marked resistance to dessication. The potentially active bacterial community changed significantly as summer dry-down progressed, then returned to pre-dry-down composition within several hours of rewetting, displaying spectacular resilience. Upon rewetting, transcript copies of bacterial rpoB genes increased consistently, reflecting rapid activity resumption. Acidobacteria and Actinobacteria were the most abundant phyla present and potentially active, and showed the largest changes in relative abundance. The relative increase (Actinobacteria) and decrease (Acidobacteria) with dry-down, and the reverse responses to rewetting reflected a differential response, which was conserved at the phylum level and consistent across sites. These contrasting desiccation-related bacterial life-strategies suggest that predicted changes in precipitation patterns may affect soil nutrient and carbon cycling by differentially impacting activity patterns of microbial communities. The ISME Journal (2013) 7, 2229–2241; doi:10.1038/ismej.2013.104; published online 4 July 2013 Subject Category: Microbial ecology and functional diversity of natural habitats Keywords: rRNA; rDNA; rpoB; pyrosequencing; qPCR; Mediterranean grassland Introduction Global climate change is predicted to alter precipitation and drought patterns, resulting in more extreme conditions, especially for Mediterranean ecosystems (IPCC, 2007), which are characterised by hot dry summers and cool wet winters. Microbial mineralization of carbon substrates that are accumulated during the summer period fuels large mineralization pulses upon soil rewetting (Birch, 1958; Borken and Matzner, 2009; Inglima et al., 2009). CO2 pulses resulting from the rewetting of Mediterranean annual grasslands after the summer dry period account for a large part of the annual carbon they Correspondence: R Barnard, INRA, UMR1347 Agroécologie, 17 rue Sully, BP 86510, Dijon 21065, France. E-mail: 4 Current address: INRA, UMR1347 Agroécologie, 17 rue Sully, BP 86510, Dijon, France. 5 These authors contributed equally to this work. Received 6 February 2013; revised 22 May 2013; accepted 28 May 2013; published online 4 July 2013 lose to the atmosphere (Xu et al., 2004; Jarvis et al., 2007). Thus, changes in dry-down patterns have potentially large consequences for these ecosystems’ nutrient and carbon budgets (Waldrop and Firestone, 2006a; Sheik et al., 2011; Vargas et al., 2012). The temporal distribution of precipitation in Mediterranean ecosystems, in which rainfall is almost entirely absent during the summer, probably selects for life-strategies to deal with the direct physiological effects of summer dry-down and sudden rewetting in the autumn. The characteristic patterns of soil water availability may select for indigenous soil microbes with physiological strategies that render them tolerant of a dynamic water potential environment, as well as of the indirect effects on water availability. Indeed, access to nutrients becomes more limited as the water film thickness is reduced by drought (Stark and Firestone, 1995); the rewetting of soils with autumn rains causes an abrupt flush of nutrients associated with the mineralization burst upon rewetting dry Microbial response to desiccation and rewetting RL Barnard et al 2230 soils (Borken and Matzner, 2009; Inglima et al., 2009). Both bacterial and fungal isolates have known strategies to survive desiccation and rewetting (Potts, 1994; Griffin, 1977), including: (i) the accumulation of compatible solutes (see review by Schimel et al., 2007); (ii) exopolysaccharide production, extensively studied in Pseudomonas sp. (Roberson and Firestone, 1992; Chang et al., 2007) and recently in Acidobacteria (Ward et al., 2009); and (iii) the production of dormant life forms such as spores. Field-based evidence of different bacterial groups displaying contrasting desiccationrelated life-strategies nevertheless remain scarce. Tolerance to desiccation may also result from morphological life form: fungi are generally considered more resistant to desiccation than bacteria (Gordon et al., 2008; de Vries et al., 2012), with hyphae that may cross air-filled soil pores to access nutrients and water. Both soil bacteria and fungi include heterotrophic microorganisms that are capable of rapid activation upon wet-up, that is, of playing a role in the mineralization burst that is responsible for the soil CO2 efflux pulse following a rewetting event (Fierer and Schimel, 2003; Placella et al., 2012). Although microbial communities have sometimes been shown to shift seasonally in water-limited systems (Waldrop and Firestone, 2006b; Clark et al., 2009; Cruz-Martinez et al., 2009), the functional or taxonomic groups that drive the microbial response to dry-down and rewetting, their associated strategies and to what extent these responses may be generalised still remain largely unclear (Placella et al., 2012). Molecular techniques based on ribosomal RNA (rRNA) allow the phylogenetic characterisation of bacterial and fungal groups that are present (as rRNA genes) and that have the capacity to actively synthesise proteins (rRNA). The abundance of rRNA has commonly been used as an indicator of activity (for example, Schippers et al., 2005; Jones and Lennon, 2010; see review by Blazewicz et al., 2013). The present study investigated changes in the present and potentially active soil bacterial and fungal communities, in three Mediterranean annual grasslands in California, over a 5-month summer dry-down p (...truncated)