A genomic perspective on stoichiometric regulation of soil carbon cycling

OPEN The ISME Journal (2017) 11, 2652–2665 www.nature.com/ismej ORIGINAL ARTICLE A genomic perspective on stoichiometric regulation of soil carbon cycling Wyatt H Hartman1, Rongzhong Ye2,3, William R Horwath2 and Susannah G Tringe1,4 1 Department of Energy, Joint Genome Institute, Walnut Creek CA, USA; 2Department of Land, Air and Water Resources, University of California, Davis CA, USA; 3Plant and Environmental Sciences Department, Clemson University, Clemson SC, USA and 4School of Natural Sciences, University of California, Merced CA, USA Similar to plant growth, soil carbon (C) cycling is constrained by the availability of nitrogen (N) and phosphorus (P). We hypothesized that stoichiometric control over soil microbial C cycling may be shaped by functional guilds with distinct nutrient substrate preferences. Across a series of rice fields spanning 5–25% soil C (N:P from 1:12 to 1:70), C turnover was best correlated with P availability and increased with experimental N addition only in lower C (mineral) soils with N:P ⩽ 16. Microbial community membership also varied with soil stoichiometry but not with N addition. Shotgun metagenome data revealed changes in community functions with increasing C turnover, including a shift from aromatic C to carbohydrate utilization accompanied by lower N uptake and P scavenging. Similar patterns of C, N and P acquisition, along with higher ribosomal RNA operon copy numbers, distinguished that microbial taxa positively correlated with C turnover. Considering such tradeoffs in genomic resource allocation patterns among taxa strengthened correlations between microbial community composition and C cycling, suggesting simplified guilds amenable to ecosystem modeling. Our results suggest that patterns of soil C turnover may reflect community-dependent metabolic shifts driven by resource allocation strategies, analogous to growth rate–stoichiometry coupling in animal and plant communities. The ISME Journal (2017) 11, 2652–2665; doi:10.1038/ismej.2017.115; published online 21 July 2017 Introduction Although microbial communities are critical to carbon (C) flow in the biosphere, ecosystem models have only recently begun to simulate variation in their metabolism in soils (Li et al., 2014; Wang et al., 2015; Weider et al., 2015). Increasingly powerful and available data on microbial community structure and function might help to better inform these efforts (McGuire and Treseder, 2010; Singh et al., 2010; Schimel and Schaeffer, 2012; Graham et al., 2016). Yet, compared with taxonomically constrained processes such as ammonia or methane oxidation (Bouskill et al., 2012; Ho et al., 2013), delineation of functional groups for decomposition in soils is challenging due to the broad distribution and functional redundancy of the relevant traits (Allison and Martiny, 2008; Schimel and Schaeffer, 2012; Berlemont and Martiny, 2013; Martiny et al., 2015). However, consideration of interactions between C and nutrient cycling by soil microbes may help clarify ecologically relevant functional guilds. For example, consistent shifts in terrestrial Correspondence: SG Tringe, Department of Energy, Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA. E-mail: Received 27 February 2017; revised 19 May 2017; accepted 25 May 2017; published online 21 July 2017 soil C turnover and retention with mineral N addition (Craine et al., 2007; Treseder, 2008) appear mediated in part by increased abundance of microbes utilizing simple C substrates, at the expense of those mining complex aromatic C and organic N (Treseder et al., 2011; Fierer et al., 2012; Ramirez et al., 2012; Cederlund et al., 2014; Amend et al., 2015). Phosphorus (P) availability can also contribute to regulation of soil C cycling, and the underlying traits for microbial P cycling could analogously be linked with traits for C and N acquisition. Although less commonly studied than soil C and N interactions, P availability may affect land C sink strength at ecosystem and global scales (Wang et al., 2007; Vitousek et al., 2010; Goll et al., 2012) and contribute to the regulation of soil C turnover rates even in nominally N-limited habitats, such as grasslands, temperate forests and leaf litter (Bradford et al., 2008; Manzoni et al., 2010; Strickland et al., 2010; Fisk et al., 2015). Soil P availability may not only affect the biomass of soil microbes (Griffiths et al., 2012; Zhang et al., 2015) but critically might also control community-scale rates of metabolism (Strickland et al., 2010; Spohn and Chodak, 2015), which could reflect underlying stoichiometric constraints at the scale of individual cells (Hartman and Richardson, 2013). Genomic stoichiometry constrains soil C cycling WH Hartman et al As posited by the growth rate hypothesis (Elser et al., 1996, 2000, 2003), cellular growth rates are linked to biomass N:P ratios by the high P demands of ribosomal RNA, which determines in part the rate of synthesis of N-rich proteins. Differentiation of organism C, N and P demands based on growth rate variation forms the foundation of Ecological Stoichiometry theory (Sterner and Elser, 2002; Vrede et al., 2004; Allen and Gillooly, 2009), enabling community shifts under different nutrient regimes to be connected with predictable alterations in ecosystem C cycling, particularly in aquatic ecosystems (Sterner and Elser, 2002; Weber and Deutsch, 2010; Follows and Dutkiewicz, 2011; Hessen et al., 2013; Mock et al., 2015). Development of a parallel framework to link stoichiometric regulation of microbial metabolism to soil C cycling at the community and ecosystem scales is highly desirable (Hall et al., 2011; Sistla and Schimel, 2012; ZechmeisterBoltenstern et al., 2015), especially given the integration of stoichiometric regulation of primary producers and decomposition into current terrestrial ecosystem models (Yang et al., 2014; Reed et al., 2015). However, the inter-relationships between soil stoichiometry, microbial communities and soil C cycling are not currently well understood. In culture, microbial growth rates are linked with cell N:P stoichiometry and ribosomal RNA content or gene copy number (Makino and Cotner, 2004; Karpinets et al., 2006; Keiblinger et al., 2010; Vieira-Silva and Rocha, 2010; Franklin et al., 2011), which can vary among bacterial lineages (Mouginot et al., 2014; Roller et al., 2016). Separately, variation or manipulation of P availability and stoichiometry in soils has been associated with shifts in microbial community composition (Güsewell and Gessner, 2009; Fanin et al., 2013; Leff et al., 2015; Spohn et al., 2015), without considering relationships to soil C cycling or metabolic differences among responsive microbes. We postulated that ecosystem-scale relationships between soil C cycling and P availability may arise due to changes in microbial metabolism, which reflect a dependence of growth rates on P availability, and are underpinned by shifts in microbial (...truncated)