Conventional and conservation tillage practices affect soil microbial co-occurrence patterns and are associated with crop yields

Highlights

• RT induced a stable microbial network than NT and MP in bulk and rhizosphere soils.

• More interactions of bacteria-fungi detected in RT while those of fungi-fungi in MP.

• MP harbored the most interactions and highest relative abundances of plant pathogens.

• RT alleviated ecological risks of plant pathogens with inefficient transformation.

• Plant pathogen negatively affected crop yields with more obvious in rhizosphere soil.

Abstract

A comprehensive understanding of the effects of tillage practices on soil microbial communities is fundamental to a better understanding of their roles in maintaining or improving the stability of agroecosystems. However, little is known regarding soil microbial co-occurrence patterns and their function in ecosystems shaped by long-term tillage practices. The goal of the present study was to investigate the impact of no-tillage (NT), reduced tillage (RT) and moldboard plow tillage (MP) practices on soil microbial interactions, central species and functional taxa as well as to investigate their associations with crop yields. The results showed that the average node degree was lower in the RT network than in the NT and MP networks of bulk and rhizosphere soils, indicating inefficient mutual effects among taxa and a more stable network structure induced by RT. Moldboard plow tillage resulted in the most fungal-fungal interactions (17.6%), while RT yielded the most bacterial-fungal interactions (32.3%) in the rhizosphere soils. The potential plant pathogens Fusarium were identified as hub node with most connections, and pathogen Sphingomonas and Clonostachys were found as central speices with those simultaneously termed as hub node and generalist in the MP network of rhizosphere soils. Intriguingly, these potential plant pathogens had negative correlations with crop yields in both bulk and rhizosphere soils, as determined by structural equation modeling (SEM). In contrast, RT might help to alleviate the ecological risks of the potential plant pathogens and increased the availability of soil nutrients mediated by central species, such as Nitrospira. These findings suggested RT as an optimal practice that could stabilize microbial network structure, alleviated the potential transmission of pathogens and finally enhance crop yields, providing a new perspective for tillage application in agroecosystems.

Introduction

Tillage is a major agricultural management practice used to promote crop production through weed control and crop residues incorporation (Das et al., 2014, Kladivko, 2001). Conventional tillage, including moldboard plow tillage (MP) with intensive mechanical disturbance, appears to deteriorate soil quality, causing soil erosion, loss of soil nutrients and degradation of soil structures (Knowler and Bradshaw, 2007, Zhang et al., 2012). Alternatively, conservation tillage practices, such as no-tillage (NT) or reduced tillage (RT), are available and have been widely adopted for their wide ranges of environmental, economic and social advantages relative to conventional tillage (Busari et al., 2015, FAO, 2014). However, a number of concerns regarding the continuous use of NT practices have arisen. Indeed, NT practices may result in (1) deeper soil compaction by impeding the proper development of crop roots; (2) difficulties with respect to weeds control due to herbicide-resistant weeds and the prevalence of stubble-borne diseases; and (3) higher denitrification leading to soil nitrogen loss (Llewellyn et al., 2002, Pittelkow et al., 2015, Puerta et al., 2019). In this context, RT has been proposed as an appropriate strategy that not only consolidates tillage functions but also manages the specific issues emerging with respect to NT practices (Chen et al., 2019, Rincon-Florez et al., 2020).

Different tillage practices significantly affect soil environments and shape the habitats of soil microorganisms (Zuber and Villamil, 2016). Prevention of soil disturbance, fungal hyphal growth is probably promoted that frequently found in the NT practice, while conventional tillage with crop residues incorporation into the soil often encourages bacterial dominance (Essel et al., 2019). Compared to conventional tillage, RT has been repeatedly reported to increase microbial biomass and diversity (Chen et al., 2020, Schmidt et al., 2019). In addition, as rhizosphere microorganisms coevolve with plant root growth, they have prominent impacts on plant nutrient uptake, soil carbon sequestration, pathogen suppression and abiotic stress tolerance (Philippot et al., 2013, Wei et al., 2015). Rhizosphere-associated studies under different tillage practices have been reported on arbuscular mycorrhizal fungi (Palla et al., 2020, Säle et al., 2015), but nutrient cycling and energy exchange in soils are collaboratively performed by multi-communities (i.e. archaea, bacteria and fungi) that exhibit inter-and intra-kingdom interactions (Shi et al., 2019). Moreover, comparative research on bulk and rhizosphere soils has rarely been conducted, and whether the effects of tillage are differential or uniform between the two soil compartments remains unclear.

Conservation tillage is typically combined with retaining a minimum of 30% crop residues on the soil surface after planting (Conservation Tillage Information Center CTIC, 2004). Crop residues at the soil-air interface are likely to be a source of plant pathogens, including crop root rot-causing soil- and stubble-borne pathogens, such as Fusarium, Pythium and Rhizoctonia (Govaerts et al., 2006, Roget et al., 1996). Wang et al. (2020a) reported that long-term NT with crop residues retention induced significantly increased abundances of Fusarium graminearum and Fusarium moniliforme relative to conventional tillage, indicating a severe risk of root rot under NT practice. In contrast, RT has been reported to impede the movement of plant pathogen spores and suppress major root disease from invasion and development in the root zone (Larkin, 2015, van Bruggen and Finckh, 2016). Empirical evidence suggests that the emergence of soil plant pathogens is a result of the relationships among pathogens, soil management and plants interfering with soil properties; however, is lacking (Sipilä et al., 2012). Therefore, these gaps urgently need to be closed by conducting integral analysis of microbial networks and functional connections.

Microbial network analysis has recently been used to reveal the mechanisms associated with patterns of community assembly, elucidate the interactions among different taxonomic groups and identify central species that significantly affect microbial ecology (Barberan et al., 2012, Faust and Raes, 2012). Recently, Banerjee et al. (2019) revealed that agronomic intensification negatively affected fungal network structure and mycorrhizal network complexity, and the abundances of keystone taxa were observed to be the highest under organic farming rather than conventional and NT practices. Wang et al. (2020b) reported that bacterial co-occurrence patterns were significantly different under plow tillage and NT, the latter of which induced a more stable bacterial network structure than plow tillage in the rhizosphere soils. However, there is a substantial dearth of information regarding the impacts of tillage practices on the network structures of multi-communities, including archaea, bacteria and fungi, and their potential cooperative or competitive interactions among inter- or intra-species in both bulk and rhizosphere soils.

The scope of this research was restricted to NT, RT and MP with the same amount of crop residues retention to elucidate the major impacts of different tillage practices on the co-occurrence patterns of soil microbial communities (i.e. archaea, bacteria and fungi) and between-taxa interactions in both bulk and rhizosphere soils. We specifically investigated (1) the variations in network parameters, species interactions and putative central species responses to NT, RT and MP; (2) the roles of functional microbes and their interactions in distinct microbial networks induced by different tillage practices; and (3) the impacts of soil properties resulting from different tillage practices on microbial networks, putative central species and functional taxa, finally on crop yields. Two hypotheses were tested in the present study: first, various tillage practices may elicit different co-occurrence patterns while altering inter- or intra-species interactions; and second, long-term MP may induce more interactions and higher relative abundances of potential plant pathogens than other tillage practices, negatively affecting on crop yields.