Positive Effects of Crop Diversity on Productivity Driven by Changes in Soil Microbial Composition

bioRxiv preprint doi: https://doi.org/10.1101/2020.11.27.401224; this version posted November 27, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Positive effects of crop diversity on productivity driven by 2 changes in soil microbial composition 3 4 Laura Stefan1, Martin Hartmann1, Nadine Engbersen1, Johan Six1, Christian Schöb1 5 1Institute of Agricultural Sciences, Department of Environmental Systems Science, ETH 6 Zurich, Zurich, Switzerland 7 Corresponding author: Laura Stefan, [email protected] 8 9 Summary 10 Intensive agriculture has major negative impacts on ecosystem diversity and functioning, 11 including that of soils. The associated reduction of soil biodiversity and essential soil functions, 12 such as nutrient cycling, can restrict plant growth and crop yield. By increasing plant diversity 13 in agricultural systems, intercropping could be a promising way to foster soil microbial 14 diversity and functioning. However, plant–microbe interactions and the extent to which they 15 influence crop yield under field conditions are still poorly understood. In this study, we 16 performed an extensive intercropping experiment using eight crop species and 40 different crop 17 mixtures to investigate how crop diversity affects soil microbial diversity and functions, and 18 whether these changes subsequently affect crop yield. Experiments were carried out in 19 mesocosms under natural conditions in Switzerland and in Spain, two countries with drastically 20 different soils and climate, and our crop communities included either one, two or four species. 21 We sampled and sequenced soil microbial DNA to assess soil microbial diversity, and measured 22 soil basal respiration as a proxy for soil activity. Results indicate that in Switzerland, increasing 23 crop diversity led to shifts in soil microbial community composition, and in particular to an 24 increase of several plant-growth promoting microbes, such as members of the bacterial phylum 25 Actinobacteria. These shifts in community composition subsequently led to a 15 and 35% 26 increase in crop yield in 2 and 4-species mixtures, respectively. This suggests that the positive 27 effects of crop diversity on crop productivity can partially be explained by changes in soil 28 microbial composition. However, the effects of crop diversity on soil microbes were relatively 29 small compared to the effects of abiotic factors such as fertilization (3 times larger) or soil 30 moisture (3 times larger). Furthermore, these processes were context-dependent: in Spain, 31 where soil resources were limited, soil microbial communities did not respond to crop diversity, 32 and their effect on crop yield was less strong. This research highlights the potential beneficial 33 role of soil microbial communities in intercropping systems, while also reflecting on the relative 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.27.401224; this version posted November 27, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 34 importance of crop diversity compared to abiotic drivers of microbiomes, thereby emphasizing 35 the context-dependence of crop–microbe relationships. 36 37 Keywords: intercropping, soil microbial communities, biodiversity–productivity 38 relationship, sustainable agriculture, annual crop yield 39 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.27.401224; this version posted November 27, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 40 1. Introduction 41 The past century has seen the emergence and the development of modern, intensive 42 agriculture that was accompanied by a strong increase in productivity per unit land area 43 (Barrios, 2007). However, the negative effects associated with this intensification now call for 44 a transformation towards more sustainable agricultural production (Tilman et al., 2011). 45 Current intensive agriculture indeed has negative effects on biodiversity (Newbold et al., 46 2015) and ecosystem functioning (Barrios, 2007), including that of soils (Gardi et al., 2013). 47 In particular, chemical inputs and the loss of crop diversity associated with intensive 48 agriculture are known to negatively affect soil biodiversity (Cavicchioli et al., 2019), with 49 consequences on soil ecosystem functioning, such as nutrient cycling, carbon storage, soil 50 structure regulation, and pest and disease control (Wall & Bardgett, 2012; Wagg et al., 2014; 51 Fanin et al., 2017). Losses of these essential soil functions can restrict plant growth and 52 subsequently crop yield (Giller, 2001; Bardgett & Van Der Putten, 2014). 53 Numerous studies demonstrated a strong link between soil microbes and plants 54 (Wardle et al., 2004; Fry et al., 2018). First, direct specific linkages between a plant species 55 and a particular type of microbe, such as symbiotic interactions, might occur (Wubs & 56 Bezemer, 2016). Moreover, plants have the ability to alter the soil chemical and physical 57 conditions (López‐Angulo et al., 2020). Some of these changes can be due to above-ground 58 mechanisms, such as litter inputs or variations in microclimate associated with plant canopy 59 cover (Trinder et al., 2009; Maestre et al., 2009; Delgado-Baquerizo et al., 2018). Others may 60 be the result of below-ground processes, such as increases in soil loosening and aeration due 61 to root growth, release of root exudates or plant signaling molecules, and changes in ion 62 uptake (Doornbos et al., 2012; Eisenhauer et al., 2017). Therefore, a greater richness of 63 plants, and subsequently, roots, would lead to a greater diversity of microhabitats, particularly 64 in the rhizosphere (Philippot et al., 2013). The resulting microhabitat heterogeneity would 65 then further enhance microbial diversity (Wardle, 2006; Eisenhauer et al., 2010), which could 66 also increase soil functioning, following the diversity-ecosystem functioning relationship 67 (Tilman et al., 2006). For instance, Steinauer (2015) showed that increasing plant diversity 68 led to a significant increase in soil microbial biomass and enzymatic activity. Similarly, 69 results from a grassland biodiversity experiment demonstrated that higher plant diversity 70 resulted in increased microbial activity and carbon storage (Lange et al., 2015). Most of these 71 studies were performed in natural grasslands; however, the extent to which the same effects 72 would arise in diversified cropping systems is still unclear. Indeed, intercropping, which is 73 defined as growing at least two crops at the same time on the same field, could be a promising 74 way to enhance soil microbial diversity and functioning by increasing plant diversity in arable 75 systems. This increase in soil diversity and functioning could then feedback on crop yield 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.27.401224; this version posted November 27, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 76 through enhanced microbial activity and nutrient mobilisation or decreased pathogen 77 accumulation (Wang et al., 2017; Bender & van der Heijden 2015; Zhou, Yu, & Wu, 2011). 78 However, despite current technological advances to study soil microbes, soil microbial 79 communities and their assembly mechanisms are still poorly understood (Van der Putten et 80 al., 2013; López‐Angulo et al., 2020). In particular, we are still unsure what soil microbes 81 respond to - e.g. plant aboveground traits, plant root traits, plant community composition, 82 plant functional diversity - and if these responses to the biotic environment are comparable to 83 the effects of abiotic conditions, such as soil moisture or nutrients. Consequently, the extent to 84 which plant–microbe interactions in soils could influence crop yield of intercropping systems 85 is still unclear. To shed light on this subject, we conducted an extensive common garden 86 experiment including eight annual crop species belonging to four functional groups, and forty 87 different crop mixtures of two and four species, in which we determined soil microbial 88 composition and measured soil respiration in addition to crop yield. Moreover, we repeated 89 the mesocosm experiment in two different countries – i.e. in Spain and Switzerland, which 90 differ drastically in terms of climate and soil, and with and without fertiliser application in a 91 fully factorial design. This experimental setup allowed us to examine the following research 92 questions: (1) How does crop diversity affect soil microbial diversity and functioning in 93 comparison to abiotic properties? (2) Are changes in soil microbial diversity and functioning 94 related to crop yield? (3) Are crop–soil microbe relationships and their effects on crop yield 95 environmentally context-dependent? We hypothesized that increasing crop diversity would 96 lead to an increase in microbial (alpha) diversity as well as changes in bacterial and fungal 97 community compositions – e.g. increases in symbionts, decomposers, or disease suppressive 98 microbes – and that these changes would have a positive effect on soil microbial activity (i.e. 99 soil basal respiration) and

Load more