DNA Stable-Isotope Probing Delineates Carbon Flows from Rice Residues into Soil Microbial Communities Depending on Fertilization

Abstract

Decomposition of crop residues in soil is mediated by microorganisms whose activities vary with fertilization. The complexity of active microorganisms and their interactions utilizing residues is impossible to disentangle without isotope applications. Thus, 13 C-labeled rice residues were employed, and DNA stable-isotope probing (DNA-SIP) combined with high-throughput sequencing was applied to identify microbes active in assimilating residue carbon (C). Manure addition strongly modified microbial community compositions involved in the C flow from rice residues. Relative abundances of the bacterial genus Lysobacter and fungal genus Syncephalis were increased, but abundances of the bacterial genus Streptomyces and fungal genus Trichoderma were decreased in soils receiving mineral fertilizers plus manure (NPKM) compared to levels in soils receiving only mineral fertilizers (NPK). Microbes involved in the flow of residue C formed a more complex network in NPKM than in NPK soils because of the necessity to decompose more diverse organic compounds. The fungal species (Jugulospora rotula and Emericellopsis terricola in NPK and NPKM soils, respectively) were identified as keystone species in the network and may significantly contribute to residue C decomposition. Most of the fungal genera in NPKM soils, especially Chaetomium, Staphylotrichum, Penicillium, and Aspergillus, responded faster to residue addition than those in NPK soils. This is connected with the changes in the composition of the rice residue during degradation and with fungal adaptation (abundance and activity) to continuous manure input. Our findings provide fundamental information about the roles of key microbial groups in residue decomposition and offer important cues on manipulating the soil microbiome for residue utilization and C sequestration in soil. IMPORTANCE Identifying and understanding the active microbial communities and interactions involved in plant residue utilization are key questions to elucidate the transformation of soil organic matter (SOM) in agricultural ecosystems. Microbial community composition responds strongly to management, but little is known about specific microbial groups involved in plant residue utilization and, consequently, microbial functions under different methods of fertilization. We combined DNA stable-isotope ( 13 C) probing and high-throughput sequencing to identify active fungal and bacterial groups degrading residues in soils after 3 years of mineral fertilization with and without manure. Manuring changed the active microbial composition and complexified microbial interactions involved in residue C flow. Most fungal genera, especially Chaetomium, Staphylotrichum, Penicillium, and Aspergillus, responded to residue addition faster in soils that historically had received manure. We generated a valuable library of microorganisms involved in plant residue utilization for future targeted research to exploit spe-

Soil Bacterial and Fungal Richness Forecast Patterns of Early Pine Litter Decomposition

“…Eurotiales , Nocardioidaceae , Hyphomicrobiaceae , Caulobacteraceae , and Methylobacteriaceae were strongly linked to the DOC cohorts based on their consistent, significant differences in relative abundance between cohorts in samples from the original soils and day 44 microcosms ( Figure 4 ). Members of these taxonomic groups are early to mid-stage decomposers of plant litter as well as fungal necromass ( Baldrian et al, 2012 ; Matulich et al, 2015 ; Brabcová et al, 2016 ; Kielak et al, 2016 ; Purahong et al, 2016 ; Bonanomi et al, 2018 ; Bani et al, 2019 ; Sauvadet et al, 2019 ; Wilhelm et al, 2019 ; Kong et al, 2020 ). The groups represent a mix of generalists ( Eurotiales , Nocardioidaceae ) and specialists with noteworthy physiological characteristics ( Hyphomicrobiaceae , Caulobacteraceae , and Methylobacteriaceae ).…”

Probabilistic Ranking Of Microbiomes Plus Taxa Selection to discover and validate microbiome function models for multiple litter decomposition studies

“…By determining the Markov blanket of the DOC node using many permutations of training data, our BN analysis rigorously searched over all features to select a minimal set of microbial genera that constrain the probability of high DOC abundance. Several of the genera identified in the Markov blanket set ( Figure 2) are known to be involved in litter decomposition either directly or indirectly [2,[27][28][29][30][31][32][33]. Of the 11 most robustly selected features, Phyllobacterium (selected in 90% of BNs) and Ensifer (selected in 70% of BNs) were the only two genera associated with high DOC; these known nitrogen-fixing bacteria are likely helpful to promote decomposition of pine litter, which is often nitrogen limited [2,29,33].…”

Fungi Outcompete Bacteria for Straw and Soil Organic Matter Mineralization

“…The following four treatments were conducted for each of the unfertilized and fertilized soils (Control, NPK, and NPK+Straw soil): (1) control with neither straw nor N fertilizer (S0+N0); (2) addition of 13 Cmaize straw (2 g kg −1 dry soil) (S+N0); (3) addition of 13 C-maize straw (2 g kg −1 dry soil) and low N (0.07 g kg −1 dry soil) (S+N1); and (4) addition of 13 C-maize straw (2 g kg −1 dry soil) and high N (0.2 g kg −1 dry soil) (S+N2). There are 12 treatments (three soil fertilization levels × four addition treatments), with three replications.…”

“…5). Straw provides more cellulose and lignin for fungi in the later stages [7,13], increased 18S rRNA gene copies thereby decreased competition with low negative correlations among fungal taxa (Fig. 2, 5; Additional File: Table S6).…”

“…Bacteria and fungi have unique preferences for straw decomposition and respond unequally to N additions [11]. Generally, bacteria are mainly involved in the utilization of easily available compounds at the initial stage of straw decomposition, while fungi have an advantage in the decomposition of recalcitrant organics (e.g., lignocellulose and cellulose) in the later stages [7,12,13]. The Proteobacteria and Firmicutes bacteria phyla were found to increase after the addition of straw and decrease with incubation time, as they are copiotrophs [14,15].…”