Life in the Wheat Litter: Effects of Future Climate on Microbiome and Function During the Early Phase of Decomposition

doi:10.21203/rs.3.rs-377061/v1

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Life in the Wheat Litter: Effects of Future Climate on Microbiome and Function During the Early Phase of Decomposition

https://doi.org/10.21203/rs.3.rs-377061/v1

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published 06 Sep, 2021

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Even though it is widely acknowledged that litter decomposition can be impacted by climate change, the feedback of the corresponding functional roles of decomposing microbes to climate change is understood to a lesser extent. Litter decomposition is linked to the corresponding functioning of the microbiome, but the feedback to climate change is so far scarcely studied. This study used a field experimental facility settled in Central Germany to analyze the effects of ambient climate vs. future climate, which is expected in 50 – 70 years, on mass loss and physicochemical parameters of wheat straw in agricultural cropland at the early phase of litter decomposition process. Additionally, the effects of climate change were assessed on microbial richness, community compositions, interactions and their functions (production of extracellular enzymes), as well as litter physicochemical factors shaping their colonization. The initial physicochemical properties of wheat litter did not change between both climate conditions, however, future climate significantly accelerated litter mass loss as compared with ambient one. Using MiSeq Illumina sequencing, we found that future climate significantly increased fungal richness and altered fungal communities over time, while bacterial communities were more resistant in wheat residues. Fungi corresponded to different physicochemical factors of litter under ambient (C, Ca²⁺ and pH) and future (C/N, N, P, K⁺, Ca²⁺ and pH) climate conditions. Moreover, a highly correlative interactions between richness of bacteria and fungi were detected under future climate. Furthermore, the co-occurrence network patterns among dominant microorganisms inhabiting wheat residues were strongly distinct between future and ambient climates. Activity of microbial β-glucosidase and N-acetylglucosaminidase in wheat straw were significantly higher under future climate. Such high enzymatic activities were coupled with a significant positive correlation between microbial (both bacteria and fungi) richness and community compositions with these two enzymatic activities only under future climate. Overall, we provide evidence that future climate significantly impacted the early-phase of wheat litter decomposition through direct effects on fungal communities and through indirect effects on microbial interactions and corresponding enzymes production.

Paleoecology

Terrestrial Ecology

wheat straw decomposition

climate change

litter physicochemical properties

hydrolytic enzymes

MiSeq Illumina sequencing

microbial community

Wheat litter incorporation into the soil is a well-established sustainable practice in modern agricultural systems [1]. Decomposition of wheat residues supports plant productivity by increasing soil organic matter and other nutrients [2]. The dynamics of the plant litter decomposition process is triggered and regulated by several factors such as litter quality, abundances and activities of soil decomposers, especially saprotrophs. Moreover, all these factors were governed by climatic conditions [3-6]. Wheat litter consists of cellulose (28–39%), hemicelluloses (23–24%), lignin (16–25%), and few contents of ashes and proteins [7]. The relative proportions of these compounds differ within plant organs and determine litter quality [8]. In cropland ecosystems, it is a common practice that only the glucan- (hemicellulose) and lignin-rich short stems (i.e., 10 cm aboveground) remain after harvest to be incorporated into the soil [7].

Microbes are the primary agents of decomposition, whereby fungi play essential roles due to their ability to produce various enzymes catalyzing breakdowns of polymeric organic plant compounds such as cellulose, hemicellulose and lignin [9]. Bacteria facilitate decomposition process directly by producing decomposing proteolytic and cellulolytic enzymes or indirectly by interacting with fungi or by increasing available nutrients for further colonizing taxa [3, 10]. Recent study reported a stronger impact of bacteria on litter decomposition rates than fungi [11]. Numerous studies have demonstrated that the microbial activities, as measured by the amount of microbial enzymes, are linked with litter decomposition rates in different ecosystems [6, 10, 12, 13]. The antagonistic or competitive relationships between litter-colonizing microbes significantly influences the quantities of these litter-degrading enzymes [10, 13]. However, the complex interaction among microbial communities, chemical composition of wheat litter, and enzyme activities remains unclear and especially under the conventional farming scenario of cropland ecosystems. In addition, the driving physicochemical factors, identity and dynamics of microorganisms associated with wheat residues in soil are still poorly documented at the early stage of decomposition. Changes of the microbial community assemblage at the early stage of decomposition determine the microbial richness and community compositions, nutrient cycling and related ecosystem functions in later stages [14, 15].

At global and regional scales, climatic factors, especially temperature and moisture, are the main driving elements of litter decomposition by affecting both the identity and activity of decomposing organisms [10, 16, 17]. A large experimental study investigated early stage litter decomposition at the biome scale (across nine biomes) showed that climatic conditions had a significant role on litter mass loss, whereby precipitation was the more influencing factor than temperature [5]. In agroecosystems, a meta-analysis reported that an increase of temperature by 2 °C was found to accelerate litter decomposition across China [18]. At local scale, high moisture and temperature due to seasonal variation were found to increase wheat litter decomposition rate [1]. Since litter decomposition is affected by temperature and moisture regimes, change in climate conditions is expected to influence such decomposition process including the combined effects of both factors, temperature and moisture. Only few studies to date have investigated these combined factors on litter decomposition. For instance, Yin et al. reported adverse effect of future climate conditions on litter decomposition rate [19]. To the best of our knowledge, the influence of future climate compared to ambient climate conditions on mass loss of wheat litter and associated microbial communities along with their enzymes activities is poorly investigated.

The present study took advantage of a field infrastructure, the Global Change Experimental Facility (GCEF), established in Germany. This facility has been designed to investigate the consequences of a predicted future climate scenario on ecosystem processes in comparison with ambient climate conditions across different land uses [20]. We performed a litter decomposition experiment in conventionally managed cropland ecosystem plots. In our preliminary work, we have demonstrated that fungal plant pathogens are highly dominant at wheat residues during the early phase of field decomposition [21]. Pathogenic fungi were accounted by ~87% of the relative abundance of total mycobiome while saprotrophs were present at relatively low abundance (1.1–3.7%) [21]. Some of these plant pathogens are reported to have litter-decomposing abilities [22]. Therefore, the aims of this present study were to compare between the influence of ambient and future climatic conditions on (i) the diversity and community composition patterns of bacteria and fungi inhabiting wheat litter during the early phase of decomposition (two months after field incorporation) (ii) the physicochemical factors corresponding with bacterial and fungal diversity and community composition; (iii) the changes of physicochemical properties of wheat litter, (iv) patterns of microbial ecosystem functions (enzyme activities) and wheat litter mass loss; (iv) the linkage among richness, community composition, physicochemical and enzyme activities at the early stage of wheat litter decomposition and (v) the interaction between plant pathogenic fungi and other microbes (bacteria and fungi). We hypothesized that (H1) patterns of microbial richness and community dynamics would differ under ambient and future climate (Fig. S1); (H2) among bacteria and fungi (total, saprotrophs, and pathogens) are different between ambient and future climate; (H3) climate change has indirect effect on microbial communities through influencing on wheat litter physicochemical; and finally (H4) direct and indirect effects of future climate on microbial communities negatively impact enzyme activities and mass loss of wheat litter during the early phase of decomposition.

Study site and experimental platform

Our study was carried out in a temperate cropland characterized by a subcontinental climate (mean temperature 8.9 °C, and mean annual rainfall of 498 mm for the period 1896–2013; mean temperature 9.8 °C, and mean annual rainfall of 516 mm for the period 1995–2014) in the Global Change Experimental Facility (GCEF), a field research station of the Helmholtz Centre for Environmental Research in Bad Lauchstädt, Saxony-Anhalt, Germany (51°22′60 N, 11°50′60 E, 118 m a.s.l.). During the study period (2018), the mean temperature was 10.8 °C with an annual rainfall of 254 mm. The GCEF (Fig. S2a) was designed to comparatively investigate the consequences of future climate and ambient climate conditions on ecosystem processes in a 50 field plots (400 m²each), with half of them subjected to ambient and future climatic conditions, respectively [20]. The future climate regime is a consensus scenario across three models (COSMO-CLM [23], REMO [24] and RCAO [25]) of climate change in Central Germany for the years 2070–2100 that manipulate both precipitation and temperature. For this, future climate plots (Fig. S2b) are equipped with mobile shelters and side panels, as well as an irrigation system, the roofs are controlled by a rain sensor. As result of continuous adjustment of irrigation or roof closing, precipitation is reduced by ~20% in summer months and increased by ~10% in spring and autumn. To simulate the increase in temperature with asymmetry between daytime and nighttime warming, we used the standard method passive nighttime warming to maintain the higher daytime temperature for increasing night temperature [26]. The shelters and panels automatically close from sundown to sunrise to increase the mean daily temperature by ~0.55 °C. The resulting changes in climate conditions before and during the study period were shown in our preliminary work [21]. Ambient climate plots are equipped with the same steel constructions (but without shelters, panels, and irrigation system) to mimic possible microclimatic effects of the experimental setup [20]. The wheat straw decomposition experiment was performed on the conventional farming plots under both ambient (five replicate plots) and future climate (five replicate plots) conditions. The conventional farming plots are characterized by a typical regional crop rotation (including winter rape, winter wheat, and winter barley) with tillage and application of mineral fertilizers and pesticides. Management details are given elsewhere [20].

Litterbag preparation, experimental design, and sampling

After harvest of winter wheat (Triticum aestivum L.), the straw left over (10 cm aboveground) was sampled from each GCEF field plot and placed in sterile plastic bags before transferred to the laboratory on ice. The wheat straw from each plot was oven-dried at 25 °C for 3 days to normalize the moisture content, and then 10 g was enclosed in a litterbag (20 × 15 cm, 5 mm mesh size) [21]. Three litterbags were returned back to each field plot (five ambient conventional farming plots and five future conventional farming plots) in mid-August 2018. Our experiment was therefore established at the end of the drought period under future conditions in summer. We evaluated the effects of future climate four years after the start of climate manipulation (the manipulation of temperature and precipitation started in April and July 2014, respectively). To simulate the natural field conditions, the litterbags were placed on the soil surface at the beginning of the experiment and following the agricultural practices (tillage) they were buried at 5 cm depth after 20 days. First sampling occurred at the onset of the experiment (0 days). The litterbags were buried at the same original location in the plots after the process of tillage in September, second sampling was done in first 30 days and the third sampling at 60 days after field incorporation. For sampling, one litterbag per plot was placed in sterile plastic bag before transferred to the laboratory on ice.

Microbial DNA Extraction, PCR, and Illumina Miseq Sequencing

Wheat straw from each bag was homogenized with the aid of liquid N₂ and were used for further analyses. DNA was extracted from 150 mg of homogenized wheat straw sample using a DNeasy PowerSoil kit (Qiagen, Valencia, CA, USA) according to the manufacturer’s instructions, then subjected to polymerase chain reaction (PCR). The V5–V7 region of the bacterial 16S rRNA gene was amplified using the following primers: BAC799F forward (5′-AACMGGATTAGATACCCKG-3′) [27] and BAC1193R reverse (5′-ACGTCATCCCCACCTTCC-3′) [28]. These bacterial primer pairs were chosen because they do not amplify the chloroplast DNA in pyrosequencing [29]. The ITS2 region of fungi was amplified using the following primers: fITS7 (5′-GTGARTCATCGAATCTTTG-3′) [30] and ITS4 (5′-TCCTCCGCTTATTGATATGC-3′) [30]. The amplification was performed in a two-step process. First amplifications were performed in 25 µL reactions with a Qiagen HotStar Hi Fidelity Polymerase Kit (Qiagen Inc., Valencia, CA, USA), 1 µL of each 5 µM primer, and 1 µL of template. Reactions were performed on ABI Veriti thermocyclers (Applied Biosytems, Carlsbad, CA, USA). The first PCR conditions were 95 °C for 5 min, then 35 cycles of 94 °C for 15 s, 54 °C for 60 s, 72 °C for 1 min, followed by one cycle of 72 °C for 10 min and 4 °C hold. Amplicons from the first stage amplification were diluted 1:10 and then used as a template in the second PCR. During the second PCR, dual indexes were attached using the Nextera XT Index Kit with the same amplification conditions as the first stage, except for 10 cycles. Amplification products were visualized with eGels (Life Technologies, Grand Island, New York) as explained by the manufacturer. Products were then pooled equimolar and each pool was size selected in two rounds using Agencourt AMPure XP (BeckmanCoulter, Indianapolis, Indiana) in a 0.75 ratio for both rounds. Size selected pools were then quantified using the Quibit 2.0 fluorometer (Life Technologies). Sequencing was performed using MiSeq (Illumina, Inc. San Diego, California) 2 × 300 bp paired-end strategy according to manufacturer`s manual.

Bioinformatic analysis

The primer sequences were trimmed from the demultiplexed raw reads using cutadapt [31]. The pair-end raw reads of bacterial and fungal datasets were merged using the simple Bayesian algorithm with a threshold of 0.6 and a minimum overlap of 20 nucleotides as implemented in PANDAseq [32]. Reads fulfilling the following criteria were remained for further analyses: a minimum length of 350 (bacteria) and 120 (fungi) nt; a minimum average quality of 29 (bacteria) or 25 (fungi) Phred score; containing homopolymers with a maximum length of 20 nt; without ambiguous nucleotides. We detected chimeric sequences using the UCHIME algorithm [33] as implemented in MOTHUR and removed from the datasets. The obtained reads were then clustered into operational taxonomic units (OTUs) using the CD-HIT-EST algorithm [34] at a threshold of 97% sequence similarity. The OTU representative sequences (defined as the most abundant sequence in each OTU) were taxonomically assigned against the reference sequences from the SILVA database v132 [35] for prokaryote 16S rRNA gene and the unite database (version unite.v7) [36] using the naive Bayesian classifier as implemented in MOTHUR [37] using the default parameters. Rare OTUs (singletons and doubletons) which potentially might originate from artificial sequences [38] were removed. The read counts were normalized to the smallest read number per sample. Therefore, the final normalized dataset without rare OTUs was used for further statistical analysis, unless otherwise stated. The ecological and metabolic functions of bacterial OTUs were predicted using FAPROTAX [39] and the functional annotation tool of prokaryotic taxa v.1.1, whereas those of fungal OTUs were predicted using FUNGuild [40].

Mass loss and physicochemical analysis of wheat straw

The dry mass of wheat straw samples from the GCEF plots was determined after oven drying at 105 °C to constant weight (mostly after 24 h), and was used for determination of mass loss at three time points (0, 30, and 60 days) under ambient and future climate regimes. Physicochemical properties were determined for total of 30 samples (10 samples for each time point where half of these are incubated under ambient and future climate conditions, respectively). Total C and N concentrations were determined by dry combustion at 1000 °C with a CHNS-Elemental Analyzer (Elementar Analysensysteme GmbH, Hanau, Germany) according to manufacturer’s protocol. Available soil phosphorus was extracted and measured according to Bray 1 method [41]. Concentration of cations (K⁺, Mg²⁺, Ca²⁺, and Na⁺) were determined by atomic absorption spectrophotometry, using a Z 5300 instrument (Hitachi—Science & Technology, Tokyo, Japan) following recommendations of the manufacturer. The pH of the wheat straw samples was measured using a WTW Multi 3510 IDS portable meter (Weilheim, Germany).

Assay of microbial enzyme activity in wheat straw

Activities of five microbial extracellular enzymes were measured in the same 30 samples of homogenized wheat straw. Of those, three are hydrolytic enzymes important for the acquisition of polymeric carbon (b-glucosidase), nitrogen (N-acetylglucosaminidase) and phosphorus (phosphatase); and two are oxidative enzymes related to the chemical modification of lignin (phenol oxidase and peroxidase) [3]. Hydrolytic and oxidative enzymes were measured based on 4-methylumbelliferone (MUB) derivatives and 3, 3′, 5, 5′-tetramethylbenzidine (TMB), respectively, as described previously [42].

Statistical analysis

Statistical analyses were performed using the PAST program v.2.17c [43] and IBM SPSS Statistics (Version 24) software. All the analyses were conducted based on five independent replicate plots of the field experiment (n = 5) with time as within plot factor. Bacterial and fungal OTU richness were calculated for each sample using the ‘diversity’ function in the PAST program. Samples rarefaction curves of fungi and bacteria are shown in Fig. S3. As the rarefaction curves indicated sufficient OTU coverage, we used the observed OTU richness directly as a proxy for bacterial and fungal diversity. Permutational multivariate analysis of variance (NPMANOVA) [44] based on Jaccard distance (permutations = 999) was performed to test the impact of sampling times and climate conditions on bacterial and fungal (including plant pathogen and saprotrophs) communities over time. Non-metric multidimensional scaling (NMDS) was used to visualize the variations of bacterial and fungal community compositions among the three sampling time points (0, 30, and 60 days), under ambient and future climate conditions, respectively. We used the presence/absence data of bacterial and fungal communities and Jaccard dissimilarity distances (permutations = 999) to perform the NMDS ordination plot as they are more reliable than relative abundance data. All physicochemical properties that significantly affected bacterial and fungal community compositions (p < 0.05) were fitted in the respective NMDS ordination plots using PAST. T-test was applied to evaluate the effect of climate on mass loss of wheat straw at 30 and 60 days under ambient and future climate conditions, respectively. Effect of climate, time and their interaction on physicochemical properties of wheat straw and on microbial enzymes activity were assessed by time-series analysis using SPSS as the data sets vary over time. With this test, climate was used as a between‐subject factor and time was used as within plot factor. We tested the correlation between bacteria and fungi (community composition and richness) and wheat straw physicochemical properties. Additionally, the correlation between microbial communities and richness and enzyme activities was investigated. For correlation analyses, Jarque-Bera test was performed to evaluate normal distribution of the datasets [45]. Pearson’s correlation and Spearman’s rank correlation were applied with normally distributed and not-normally distributed datasets, respectively. Due to the significance of fungal plant pathogens in field-incorporated wheat straw, we aimed to characterize the interactions between these pathogens and other microorganisms colonizing wheat residues. We performed ecological network analysis (ENA) using Spearman’s rank correlations (P < 0.05) for ambient and future climate conditions, separately. The ecological networks of potential interacting taxa were visualized using cytoscape 3.0.2. [46]. Network properties were calculated using Network Analyser as implemented in cytoscape. These correlation networks included nodes that consisted of plant pathogenic fungi and fungal and bacterial OTUs as a proxy for ‘species’, while the edges represented the correlative relations among the OTUs [47]. Microbial hubs are defined as strongly interconnected taxa, which can have a severe effect on microbial community compositions and networks if they were removed [48].

A total of 237,675 quality-ﬁltered bacterial 16S rRNA gene and 585,217 fungal ITS sequence reads were obtained, resulting in rarefied 5,104 bacterial and 9,020 fungal sequence reads per sample. Bacterial communities under both ambient and future climate regimes were dominated by Proteobacteria (85 - 86% of the total bacterial sequences reads), which were mostly assigned to Gammaproteobacteria (95 - 96%) and Alphaproteobacteria (4-5%), and Actinobacteria (11 - 13% of the total bacterial sequences, with 89 - 92% assigned to Micrococcales). Fungal communities were dominated by Ascomycota (98.3% of total fungal sequences reads), while Basidiomycota was rare (1.7% of all fungal sequences) at the early phase of wheat litter decomposition. Information on bacterial and fungal taxonomic compositions are provided in Figs. S4 and S5. The datasets comprised of 2,737 bacterial and 275 fungal OTUs. 15.9 % and 28.7 % of bacterial and fungal OTUs, respectively, were found only under the future climate conditions.

Impact of future climate conditions, decomposition time and their interaction on microbial richness in wheat litter.

We investigated the impact of climate, decomposition time and their interaction on bacterial and fungal OTU richness (Fig. S6 a, b). Future climate conditions significantly increased only the richness of fungal OTUs (F = 16.32, p < 0.001) in wheat residues. Both bacterial (F = 27.80, p < 0.001) and fungal (F = 13.60, p < 0.001) OTU richness increased over decomposition time.

Microbial community composition in wheat litter over time in correspondence to future climate conditions

The influences of climate conditions and sampling times on the bacterial and fungal community composition colonizing wheat litter were examined at the OTU level (97% identity) (Table S1). NPMANOVA based Jaccard distances revealed that future climate significantly (F = 1.45, p = 0.015; Table S1) altered only the fungal community composition. Time significantly shaped both bacterial (F = 2.25, p = 0.001; Fig. 1a, b) and fungal (F = 1.76, p = 0.001; Fig.2 a, b) community composition. However, the NPMANOVA corroborated by NMDS plots revealed that interaction between climate conditions and time significantly affected only fungal community composition (F = 1.33, p = 0.011) (Fig. 1a, b; Fig. 2a, b; Table S1). Fungal community composition showed a succession of colonizers over sampling time only at the future climate conditions, as we recognized a distinct community pattern in each single sampling time (Fig. 2a). On the other hand, the fungal community composition at ambient climate regime did not significantly alter over time (Fig. 2b). The most abundant (>1% of the relative abundance in at least one of the sampling times) taxa present in the early phase of decomposition reflect diverse metabolic and ecological function patterns with a shift in their relative abundance among sampling times (bacteria, Fig. 1c; fungi, Fig. 2c). Some taxa were highly abundant at all time points under both climatic conditions such as Pantoea (bacterial OTU1), Massilia (bacterial OTU2), Mycosphaerella tassiana (fungal OTU1), and Alternaria hordeicola (fungal OTU2).

Co-occurrence networks between plant pathogenic fungi and other microorganisms are dissimilar between ambient and future climate conditions

First, we performed a correlation analysis to explore the influence of climate changes on the co-occurrence between bacteria and total fungi as well as dominant fungal guilds (saprotrophic and plant pathogenic fungi) (Table 1). Bacterial richness significantly correlated with total and saprotrophic fungal richness under both climate conditions, however the correlation under future climate conditions was clearly stronger (R = 0.91-0.92, p < 0.001) as compared to the ambient one (R = 0.54 – 0.57, p < 0.05). Moreover, bacterial richness correlated with plant pathogenic fungi only under future climate (R = 0.55, p < 0.05). Due to the economic significance of plant pathogenic fungi colonizing field-incorporated wheat litter, we performed ecological network analyses (ENA) to predict the potential interactions among the dominant plant pathogenic fungi (~87% of total fungal sequence read abundance) and further members of the microbial communities under each climate condition, separately (Fig. 3). Plant pathogenic fungi obtained a hub topological role in both climate regimes, however, represented with various taxa under each climate-specific network. The network of ambient climate conditions consisted of 91 microbes (nodes) and 129 correlations (edges) and highest number of connections were detected between the fungal pathogens, Mycosphaerella tassiana and Neosetophoma rosigena with other microbes (Fig. 3a). The network of future climate conditions consisted of 100 nodes and 170 correlations and the highest number of connections were between the fungal pathogens Pseudopithomyces rosae and Gibellulopsis piscis with other microbes (Fig. 3b, Table S2).

Effect of climate change and time on mass loss, physicochemical properties, and microbial enzyme activities of wheat litter

Future climate conditions significantly accelerated the mass loss of wheat litter at the early phase of decomposition. After 60 days of field incorporation, wheat straw dry matter was reduced by 15.8% under future climate, compared to 10.6% under the ambient one (t = 2.68; p < 0.05) (Fig. 4a). With regards to the physicochemical properties of litter (Figs. 4b-i), slow nutrient release was observed during the early phase of decomposition, except for N (F = 8.09, p < 0.001) and Mg²⁺ (F = 3.51, p < 0.05) that showed a significant reduction after 60 days of field incorporation. Immobilization of P and Ca²⁺ was clearly observed as the concentrations of both elements increased over time under future climate conditions. Moreover, these conditions had a neglectable influence on changes of chemical composition of litter. Although we detected a higher release of C and K⁺ at 30 days sampling under future climate (during summer drought), a bioaccumulation of both elements was observed at 60 days (increased precipitation in autumn) to resemble those under ambient climate conditions.

Analysis of microbial extracellular hydrolytic enzyme activities in wheat litter revealed a significant increase of ß- glucosidase (F = 15.30, p < 0.001) and N-acetylglucosaminidase (F = 16.85, p < 0.001) over time (Fig. 5a-c). Both enzymes reached the highest activity at 60 days sampling under future climate conditions. Almost no activity of oxidative enzymes was detected during the early phase of straw decomposition under both climate conditions (Fig. 5d, e).

Influence of future climate conditions on the relationship between resident microbes (richness and community composition) and physicochemical properties as well as microbial extracellular enzymes in wheat litter

A correlation analysis was performed to elucidate the potential link between wheat litter physicochemical properties and community compositions and richness of litter-resident microbes under both climate conditions (Table 2). The contribution of future climate to influence the factors shaping microbial communities in wheat straw was highly recognized for fungi. For instance, total fungal richness and community composition were significantly (P < 0.05) correlated with increased C, Ca²⁺ and pH under ambient climate conditions, while it were also correlated with C/N, N, P, K⁺, Ca²⁺ and pH under future climate conditions (Table 2; Fig. 2a, b). The same observation was also found in case of saprotrophic and plant pathogenic fungi. For bacteria, there were a positive correlation between the richness and community composition and common (Ca²⁺, C/N, N, pH), but also less differentiated (P) factors in correspondence to climate condition (Table 2; Fig. 3a, b).

A correlation analysis was performed between microbial community compositions and richness with enzyme activities under both climate conditions (Table 3) to be considered as a potential prediction of ecosystem functions under ambient and future climate conditions. Climatic conditions significantly influenced the correlation between both bacterial and fungal community compositions and enzyme activities in wheat residues. For instance, the bacterial and total fungal community compositions and richness were significantly correlated (p < 0.05) with phosphatase activity under ambient climate conditions, while correlated with higher ß-glucosidase and N-acetylglucosaminidase activities under future climate conditions. Similarly, saprotrophic and pathogenic fungi were found to correlate with ß- glucosidase and N-acetylglucosaminidase under future climate.

Future climate alters fungal communities and impacts microbe-microbe interactions in wheat litter

Our work highlights major changes in the bacterial and fungal richness and community compositions due to projected climate changes at the early phase of wheat litter decomposition (hypothesis 1). Future climate did not significantly influence bacterial richness or community composition in wheat residues. Additionally, bacterial communities correlated with the same physicochemical factors of wheat litter under both ambient and future climate conditions. In contrast, future climate significantly altered fungal community composition and shaped its patterns over time with increasing richness. Moreover, future climate conditions significantly altered the correlation between fungi and wheat litter physicochemical factors (hypotheses 1 and 3). Our results proved the sensitivity and obvious turnover in the community composition of fungi-colonizing litter due to climate changes. Our result is in line with the recent global investigation of fungal distribution in soils across biomes, which revealed that temperature and precipitation are the primary and secondary elements of climate variables explaining fungal variation, respectively [49]. The impact of future climate on microbial interactions is so far less studied. Here, we found that climate change did not only affect fungal communities but also simultaneously impacted the co-occurrence patterns among microorganisms. We detected a stronger correlative interactions between species richness under future climate conditions. In addition, the use of co-occurrence networks in our study highlighted the influence of climate change on the interaction between bacteria, saprotrophic fungi and pathogenic fungi. The microbial networks showed similar complexity under both ambient and future conditions. Also, pathogenic fungi were discerned as keystone taxa. However, the identity of those taxa has been altered in correspondence to climate conditions. This could be explained by competition of heat-tolerant and susceptible taxa due to warm climate compared to sensitive taxa. Additionally, associated drought conditions amplifies the differential temperature sensitivity of microbes as reported before [50].

Future climate positively affects mass loss of wheat residues at early phase of decomposition.

We expected that the reduction of precipitation during the summer period coupled with higher temperature of future climate might cause a significant reduction of litter decomposition as demonstrated by a previous study from the same field plots on oat litter decomposition [19]. However, in contrast to our hypothesis, we found faster mass loss of wheat litter under future (˜15%) climate as compared to the ambient one (˜10%). The discrepancy between the results from our study and the previous one could be partly explained by different season when we measured the mass loss. We settled our experiment on mid-summer period while the mass loss was measured during autumn. Therefore, we covered the period of increased precipitation together with increasing soil temperature, which coincidences with a faster decomposition rate. Thus, the decomposition rate in our study is indicative only for a certain period of the year when future climate might increase decomposition. On the other hand, Yin et al. (2019) investigated decomposition rate across two complete years passing by increasing precipitation during spring followed by summer drought [19]. As per the findings from both studies, we hypothesize that the positive effect of future climate on early decomposition stage of wheat litter, at the present study, may become neglected at late stages of litter decomposition. Other reason of contradicted results could be attributed to the litter quality. In our study, wheat stem samples from 10 cm above ground were used while in previous study, oat plants with stems and leaves were used [19]. Wheat straw have more lignin and hemicellulose than oat straw resulting in slower decomposition rates for wheat [51]. On the other hand, it is clear that the mass loss values of wheat stem were only between 10 – 15% after 60 days incubation, which is much lower than the mass loss as reported in other studies [52]. Wheat litter mass loss reported to be 80% after incorporation in rice–wheat rotation system. This result was explained by the high soil moisture content and temperature during the rice season. Therefore, climate conditions are considered the predominant factor when litter quality is similar.

Climate drives the contribution of microbes to the litter decomposition process

Beside other soil biota, microorganisms consider the engines of plant litter decomposition process. Future climate conditions positively affected mass loss of wheat litter at early stage of decomposition directly by altering fungal community composition and richness as reported before [11]. In addition, we also detected other effects of climate on microbial activities that contributed to the decomposition process. At the early phase of litter decomposition, labial compounds like simple sugars and amino acids are normally consumed first by microbes with the aid of hydrolytic enzyme activities [3]. This corresponded to the strong positive correlation between microbial communities (both fungi and bacteria) to ß-glucosidase and N-acetylglucosaminidase enzymes activity only under future climate conditions. We also showed that a more complex compound such as lignin may not sufficiently decompose at early phase as lignin degrading fungi were rarely detected and oxidative enzyme activities were neglectable in all samples. Though, future climate conditions had no significant direct effect on initial wheat straw physicochemical factors (hypothesis 2), its interaction with sampling time significantly affected enzyme activities (hypothesis 3). Decomposition process of plant materials is known to be regulated by fungal-fungal interactions [9] as well as by cross-kingdom relationships between fungi and bacteria [3, 53]. Therefore, changing of plant pathogenic fungal-bacterial and plant pathogenic fungal-fungal and pathogen-pathogen interactions may also be responsible for the different proportions of wheat litter mass loss under future and ambient climate conditions. The majority of plant pathogenic fungi that highly dominate in the early decomposition stage of wheat residue (˜87% of total detected sequences) in this study have been reported to live as decomposers and some of them are even listed as efficient cellulose decomposers [54]. In a word, our study reported that future climate changes shift the fungal community composition and richness over time leading to altering interactions among microbial taxa and hence alternate the corresponding function (litter decomposition) of the ecosystem.

This study provides the first comprehensive view of microbiome (including both bacteria and fungi) associated with the early stage of wheat residue decomposition in ambient and future climatic conditions using high-throughput DNA sequencing techniques. The strategy developed here can be viewed as a proof-of-concept focusing on wheat residues as a particularly microbial rich ecological compartment, with various patterns of diversity-structure-ecosystem functioning of fungal and bacterial taxa colonizing wheat straw under ambient and future climate treatments. Fungal communities associated with early phase of wheat residue response much stronger to the future climate change than bacterial communities. Our findings pave the way for a deeper understanding of the complex interactions among pathogens, and other microbial communities as well as effect of climate change on decomposition rate via the microbes and their associated ecosystem functions.

Funding: The next generation sequencing cost was covered by personal research budgets of W.P. from the Helmholtz Centre for Environmental Research - HFZ. S.F.M.W. is supported financially by the Egyptian Scholarship (Ministry of Higher Education, External Missions sector).

Conflicts of Interest:

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Availability of data and material

The bacterial 16S and fungal ITS2 raw read sequence datasets were deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) under bioproject number PRJNA700837.

Reviewer link:

https://dataview.ncbi.nlm.nih.gov/object/PRJNA700837?reviewer=31u0unp5giun4d8l1mo2m4fsq0

Author’s Contributions: Conceptualization, W.P. and F.B.; Coordination of GCEF platform, M.S.; Field experimental setup, S.F.M.W., B.T., C.S. and W.P.; Molecular work, S.F.M.W., B.T. , S.H. and C.S.; Bioinformatics, S.F.M.W.; Chemical analyses, Y.W.; Data analysis, S.H., W.P. and S.F.M.W.; Resources, F.B., W.P. and Y.W.; Data curation, S.F.M.W.; Visualization, S.H., W.P. and S.F.M.W.; Writing—Original draft preparation, S.H. and W.P.; Writing—review and editing, S.F.M.W., W.P., F.B., M.S., M.N. and Y.W.; Supervision, W.P.; Funding acquisition, W.P., Y.W. and F.B.

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Acknowledgements

We thank the Helmholtz Association, the Federal Ministry of Education and Research, the State Ministry of Science and Economy of Saxony-Anhalt, and the State Ministry for Higher Education, Research and the Arts Saxony for funding the Global Change Experimental Facility (GCEF) project. We also thank the staff of the Bad Lauchstädt Experimental Research Station (especially Ines Merbach and Konrad Kirsch) for their work in maintaining the plots and infrastructures of the GCEF, and Dr. Stefan Klotz, Dr. Harald Auge, and Dr. Thomas Reitz for their roles in setting up the GCEF. The sequencing data were analyzed at the High-Performance Computing (HPC) Cluster EVE, a joint effort between the Helmholtz Centre for Environmental Research - UFZ and the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig.

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Life in the Wheat Litter: Effects of Future Climate on Microbiome and Function During the Early Phase of Decomposition

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