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Article

Inconsistent Response of Abundant and Rare Bacterial Communities to the Developmental Chronosequence of Pinus massoniana

by
Qianbin Cao
,
Yunchao Zhou
*,
Hui Zhao
and
Yunxing Bai
Institute for Forest Resources and Environment of Guizhou, Key Laboratory of Forest Cultivation in Plateau Mountain of Guizhou Province, College of Forestry, Guizhou University, Guiyang 550025, China
*
Author to whom correspondence should be addressed.
Forests 2022, 13(11), 1904; https://doi.org/10.3390/f13111904
Submission received: 5 October 2022 / Revised: 8 November 2022 / Accepted: 8 November 2022 / Published: 12 November 2022
(This article belongs to the Special Issue Biodiversity-Ecosystem Functioning Relationships in Forest Ecosystems)
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Abstract

:
There are differences in the environmental adaptability and regulation of nutrient cycling between abundant and rare bacterial communities during the development of planted forest ecosystems. In this study, we aimed to elucidate the relationships between the soil characteristics and the composition and diversity of abundant and rare bacteria across a chronosequence (i.e., 13-yr, 25-yr, 38-yr, 58-yr-old stands) of Pinus massoniana. Abundant bacterial OTUs, richness, and Shannon index showed a different variation with stand age compared with the rare taxa bacterial community. Both abundant and rare bacterial communities showed significant differences between the 13-yr and 25-yr-old stands, but were similar in the 38-yr and 58-yr-old stands. The dominant phyla were Acidobacteria, Proteobacteria, Chloroflexi, Actinobacteria, and Planctomycetes in both abundant and rare taxa. However, the same phylum of abundant and rare taxa was inconsistent across the four forest ages. Network analysis further demonstrated that rare taxa had a greater network scale and complexity than abundant taxa, which may contribute to buffering the environmental stress. The Mantel test showed that soil pH, nitrogen pool (i.e., MBN, NH4+, NAlkali), and enzyme activities were the key factors that were associated with the changes in abundant bacterial diversity and structure during the development of P. massoniana. However, more soil variables (i.e., pH, SW, MBN, NH4+, NAlkali, AP, nitrite reductase, and sucrase) regulated the rare bacterial communities. Our results indicate that rare taxa are important contributors to soil bacterial community diversity, and their community dynamics responded to changes in soil physicochemical properties significantly distinct from the abundant taxa. We suggest that future studies should focus more on the response of different taxa subcommunities, rather than on the community as a whole, when studying the changes in microbial community dynamics.

1. Introduction

Coniferous forests, as one of the most widely distributed silvicultural and timber plantations around the world, are facing a decline in soil multi-nutrient supply capacity and net primary productivity [1,2,3]. Soil microorganisms may shape the development of plantation forests through altering the release and supply of available nutrients such as soil carbon (C), nitrogen (N), and phosphorus (P) from organic matter decomposition and mineralization processes [4]. Therefore, changes in the soil microbial community diversity and composition with plantation development may largely alter the plantation composition [5,6]. The development of forest can in turn alter the diversity of understory vegetation, litter, and root exudates to reshape the soil microbial community [2,7]. Large amounts of recalcitrant litter that contain lipids, lignin, and cellulose are accumulated with coniferous forest growth, and results in the transition of soil microorganisms from copiotrophic to oligotrophic groups [8,9]. In addition, the increase in fungal richness with coniferous forest development may force the bacterial community to produce more specific extracellular enzymes to mobilize their required nutrients [3,10]. For example, soil sucrase has an important role in promoting microbial organism decomposition, while soil urease and nitrate reductase plays a key role in regulating soil N cycling [10]. Therefore, understanding the changes in soil microbial communities and soil enzyme activities and their relationships is essential for understanding the decrease in nutrient supply capacity and productivity during the development of plantation forests [11]. However, there is limited information and attention to the soil bacterial community dynamics during coniferous forest development compared to the fungal community.
Soil bacteria account for approximately 80% of the total soil microorganisms in both the abundance and species, and have crucial roles in regulating the soil C, N, and P cycles [8,12]. In a natural ecosystem, however, bacterial species and abundance are distributed unevenly. For example, “rare” bacteria are lower in abundance but diverse in species and usually show higher genetic and functional diversity. They may play a more important role in maintaining the balance of ecosystem function than the “abundant” taxa, which have a higher abundance but a smaller number of species [13,14]. Rare taxa are also a large “bank” for soil microbial species and functional diversity maintenance [15,16]. For example, Jousset et al. [14] found that the functional redundancy mediated by rare bacterial taxa maintained the whole eco-balance, even though some core bacteria were extinct. Therefore, changes in the soil physicochemical properties may have a more significant effect on rare taxa than abundant bacterial communities [17,18,19]. In addition, thousands of bacterial species that are present at the same site can interact and influence each other in ways such as mutualism, parasitism, predation, symbiosis, or competition [20]. These community interactions are tightly correlated with the niche width of abundant and rare taxa [21,22]. In addition, differences in the response of abundant and rare bacterial communities within species interactions to changes in soil physicochemical properties, which may be the endogenous reasons for changes in soil ecosystem function during the development of plantation forests [23,23]. However, whether the co-occurrence patterns are consistent between rare and abundant soil bacteria during the plantation development is still unclear.
As a pioneer and high-speed growing tree species in southern China, Pinus massoniana accounts for over 4% of the total area in Chinese plantations [24]. However, P. massoniana is threatened by sustainable productivity decline, pests, and diseases, which are incompatible with the sustainable development of the P. massoniana industry [25,26]. This problem may also be a common issue for the global coniferous forestry [2,10]. Based on the high-throughput sequencing analysis, we aimed to elucidate the relationships between soil physicochemical properties and abundant and rare bacteria composition, and diversity across a chronosequence (i.e., 13, 25, 38, and 58-yr-old) of P. massoniana in southern China. In addition, the Functional Annotation of Prokaryotic Taxa (FAPROTAX) was used to speculate on potential functional changes mediated by abundant and rare bacteria during the development of P. massoniana. We aimed to answer the following questions: (i) Whether the structure and diversity of different soil bacterial subcommunities are consistent across stand ages? (ii) What are the changes in the co-occurrence patterns of abundant and rare taxonomic bacteria in the development of P. massoniana? (iii) Which factors dominate the community changes of abundant or rare taxonomic bacteria during the development of a P. massoniana plantation? Our results can help to clarify the reasons for the decline in the nutrient supply and sustainable productivity of Pinus plantations and provide a scientific reference for the sustainable development and intensive management policies for plantation forests.

2. Material and Methods

2.1. Study Region

This study was conducted in the Mengguan National Forest Farm (106°44′20′′ E, 26°29′35′′ N), Guizhou Academy of Sciences, China. This area has a subtropical monsoon climate. The mean annual precipitation and temperature are 1198 mm and 15.2 °C, respectively. The soil group is classified as yellow soil according to the China Soil taxonomy. In 1959, 1979, 1992, and 2004, this forest farm established a P. massoniana Lamb plantation after clearcutting, respectively. The shrub layer consisted of Rubus pirifolius Smith and Mallotuss japonicus. The herb layer was dominated by Imperata cylindrica, Dicranopteris dichotoma, and Pteridium aquilinum. Basic information of P. massoniana has been reported by Zhao et al. [27]. In general, the average height was 8~22 m, and the diameter at breast height was 12~36 cm. The altitude range is about 1200~1260 m, and the slope is 10~22°. Forestry management practice (e.g., fertilization) is consistent. Thus, similar conditions were guaranteed during P. massoniana development.

2.2. Soil Sampling and Physicochemical Analysis

At each stand age (i.e., 13, 25, 38, and 58-yr-old), three 20 × 20 m sites (50 m apart) were randomly set in August 2017. A total of 60 soil samples (i.e., four stands age × three sites × five replicate soil cores (Ø 5 cm)) were sampled at a depth of 0–10 cm. After removing the roots and stones, the replicated soil cores from the three sites were mixed separately to generate the final soil samples and packed in labeled sterile Ziplock bags. All samples were stored at 4 °C in ice boxes and transported to the laboratory for analysis as soon as possible. Each soil sample was divided into three parts: one was refrigerated at −80 °C for soil bacterial sequencing, microbial carbon, and microbial nitrogen content analysis; the second was air-dried and passed through a 2 mm sieve for soil pH, total nitrogen (TN) and soil organic carbon (SOC) determination; and the third was used to determine the soil water, NH4+, and NO3− contents.
Alkali-hydrolyzable nitrogen, total potassium (TK), total potassium (TK), available potassium (AK), total phosphorus (TP), and available phosphorus (AP) were determined according to Bao (28). Briefly, the soil alkali-hydrolyzable nitrogen concentration was determined by alkaline diffusion. Total potassium (TK) and available potassium (AK) concentrations were measured by a flame photometer (FP6410, Shanghai Precision Instrument Co. Ltd. Shanghai, China). Total phosphorus (TP) and available phosphorus (AP) concentrations were determined by a Mo-Sb colorimetric method [28]. Soil microbial carbon (MBC) and microbial nitrogen (MBN) were extracted by chloroform fumigation [29], and their concentrations were determined by oil bath heating and the ninhydrin colorimetric method, respectively. Methods and data used to determine the soil water content, pH, SOC, TN, NH4+, and NO3− concentrations are available in the report by Zhao et al. [27].
Soil urease, sucrase, and nitrite reductase were analyzed by 5 g of fresh soil incubated in a dark Biochemical Incubator (Guangzhi Biochemical Incubator, Guangdong, China) at 30 °C, respectively. Soil urease was determined by the phenol-hypochlorite colorimetric method, and the activity was expressed as milligrams of NH4+ in 1 g of soil within 24 h. Sucrase was determined by the 3,5-dinitrosalicylic acid colorimetric method, and the activity was expressed as milligrams of glucose in 1 g of soil within 24 h. Nitrite reductase was determined by the sulfonamide naphthalene ethylenediamine hydrochloride colorimetric method, and the activity was expressed as NO2− concentration in 1 g of soil within 24 h.

2.3. DNA Extraction, Amplification, and Sequencing

DNA extraction was performed with 0.5 g of fresh soil according to the instructions provided in the E. Z. N. A.® Soil DNA Kit (Omega, GA, USA). The purity and integrity of the extracted DNA were determined by 1% agarose gel electrophoresis on a NanoDrop ND-1000 platform. The V3-V4 region of the bacterial 16S rRNA was amplified and sequenced using the 338F (5′-ACTCCTACGGGAGGCAGCAG-3′)/806R (5′-GGACTACHVGGGTWTCTAAT-3′) primer pair [30] on the Illumina MiSeq platform (PE300, Shanghai Personal Biotechnology Co. Ltd. Shanghai, China). The PCR amplification process was as follows: predenaturation at 95 °C for 5 min, denaturation at 94 °C for 40 s, annealing at 58 °C for 30 s, and extension at 72 °C for 60 s. The above steps were continued for 30 cycles followed by extension at 72 °C for 5 min to the end. The PCR amplification reaction was performed using a 50 μL buffer system that contained 4 μL of DNA template, 0.2 μL each of the forward (20 ng/μL) and reverse (50 ng/μL) primers, and 25 μL of Premix Taq DNA polymerase (5 U μL−1) (TaKaRa, Dalian, China); the remaining volume of solution was made up with double-distilled water. The original FASTQ files were screened and spliced in QIIME (version 1.9.0). After removing chimeras for sequence comparison, the operational taxonomic units (OTUs) were classified based on a 97% similarity threshold [31]. Finally, the representative sequence of each OTU was assigned according to the RDP database (RDP Release 11.5). The sequencing results can be viewed in the NCBI database with accession number PRJNA491760.

2.4. Data Analyses

The normality and variance homogeneity of data were tested with Shapiro–Wilk normality and Bartlett function before analysis, respectively. When the assumptions were not met, the data were ln(x + 1) transformed. One-way ANOVAs were used to compare the soil physicochemical properties and enzyme activities among the stand ages. The Duncan test was used for multiple comparisons among stand ages.
In this study, OTUs with a relative abundance above 0.01% were defined as “abundant” taxa, and those with a relative abundance below 0.01% were defined as “rare” taxa [32]. To compare the alpha diversity of abundant and rare taxa across stand ages, the picante package was used to calculate the richness and Shannon index of OTUs. Principal coordinates analysis (PCoA) based on the Vegan package (2.5-7) was used to assess the variation in the β-diversity of abundant and rare OTUs. The differences in bacterial communities across different stand ages were examined by permutational multivariate analysis of variance (PERMANOVA).
Network analysis was used to assess the co-occurrence patterns of abundant and rare soil bacterial taxa at different stand ages. In this study, Spearman correlation coefficients >0.65 and p < 0.001 were used to construct the co-occurrence networks. Spearman correlation coefficients between OTUs were calculated using the WGCNA package and p-values were corrected using the false discovery rate (FDR). The features of the networks were calculated in the igraph package in R, and network visualization was performed in the Gephi platform (version 0.9.2).
FAPROTAX (Functional Annotation of Prokaryotic Taxa) was used to infer the bacterial community functions during P. massoniana development [33]. Based on the OTU abundance table and OTU taxonomy annotation table, we obtained the relevant ecological functions of OTUs in the ImageGP (http://www.ehbio.com/) platform (12 August 2020). We counted the number of abundant and rare taxa potential function OTUs in different stand ages individually. Principal component analysis (PCA) was used to characterize the abundant and rare taxa function changes during P. massoniana development.
To assess the main soil physicochemical variables associated with shifts in the diversity and structure of abundant and rare taxa and their mediated functions, the Mantel test was conducted with the Vegan package. Relationships between changes in alpha-diversity (i.e., Shannon) and beta-diversity (i.e., PCoA1) of the abundant and rare bacterial communities and soil nutrient stoichiometry were assessed using Spearman’s correlation, with p-values corrected using FDR. All statistical analyses were performed in R (version 4.1.2).

3. Results

3.1. Variations in Soil Variables

The soil physicochemical properties and enzyme activities varied within the stand ages (Table 1, p < 0.05 or 0.01). In general, young stands (i.e., 13-yr and 25-yr-old) have a higher soil nutrient content than the old stands (i.e., 38-yr and 58-yr-old). During the plantation development from a 13-yr to 58-yr-old stand, soil nutrient content decreased from 2% to 72%. The highest MBC, TP, AP, and TK contents were in the 13-yr-old stand, while the MBN, N alkali, and AK contents were in the 25-yr-old stand.
Soil enzyme activity varied significantly along the developmental time series of P. massoniana (Table 1). The highest nitrite reductase and urease enzyme activities were in the 25-yr old stand, while the invertase enzyme was in the 13-yr-old stand. From the 13-yr to 58-yr-old stand, the mean soil enzyme activity decreased from 87% to 31%.

3.2. Characteristics of Abundant and Rare Bacterial Taxa

In general, 1423, 1897, 1486, and 1632 bacterial OTUs were obtained from the 13-yr, 25-yr, 38-yr, and 58-yr-old stands, respectively. The bacterial OTU richness increased with forest age, while the Shannon index decreased. The relative abundance of rare bacteria was below 0.01%, but their OTU richness was over 72% of the total richness across four stand ages (Figure 1A). Abundant bacterial OTU richness showed a weak U-shaped variation with stand age, while rare bacterial OTU richness increased from the 13-yr to 25-yr, decreased in 38-yr, and increased in the 58-yr old stand. The lowest value of OTU richness for rare taxa and abundant taxa were in the 13-yr and 25-yr-old stand, respectively (Figure 1A). The Shannon index for rare bacteria increased with forest age, but the abundant bacterial Shannon index increased from 13-yr to 25-yr, and there was no significant difference from 3the 8-yr to 58-yr old stand (Figure 1B).
The dominant phyla of abundant and rare taxa were Acidobacteria, Proteobacteria, Chloroflexi, Actinobacteria, and Planctomycetes (Figure 1C,D). Although there was a similar trend that occurred in the Acidobacteria, Proteobacteria, Chloroflexi, and Planctomycetes between the abundant and rare taxa along with increasing forest age. However, these changes varied with the phyla. For example, the relative abundance of Acidobacteria decreased by about 50% in both abundant and rare taxa from the 13-yr to 25-yr stand, followed by an increase in stand age. However, from 13-yr to 25-yr, the relative abundance of Proteobacteria increased by 40% and 30% for the abundant and rare taxa, respectively, but then decreased with stand age. In addition, the variations in abundant and rare taxa in the same phylum were also inconsistent across the four forest ages. For example, the relative abundance of abundant taxa of Actinobacteria decreased by 31% from 13-yr to 25-yr, followed by an increase in stand age. However, from 13-yr to 25-yr, the relative abundance of Actinobacteria increased by 20% for the rare taxa, and the highest value was also found in the 25-yr stand, and then even increased with stand age. In addition, there was a special phylum for abundant and rare taxa (i.e., Nitrospira and Chlamydiae, respectively). The highest value of the abundance of Nitrospira was observed in the 25-yr-old stand, while Chlamydiae was observed in the 38-yr stand.
Significant differences in the soil bacterial communities among different forest ages were revealed by PCoA (Figure 2; p < 0.001). Both abundant and rare bacterial communities showed a significant distinction between 13-yr and 25-yr, but the s38-yr and stands 58-yr were similar (Figure 2). The PCoA revealed a total of 86.4% variation in the abundant bacterial community along with the increase in stand age, but the rare bacterial community was 55%.

3.3. Co-Occurrence Patterns in Abundant and Rare Bacterial Taxa

Based on the Spearman correlation coefficients (|R| > 0.65, p < 0.001), we constructed the co-occurrence networks of abundant and rare bacterial OTUs (Figure 3). The counts of positive correlations in the co-occurrence networks of both abundant and rare bacteria were over 95%. This indicated that cooperation within abundant or rare taxonomic bacterial communities could contribute to resisting environmental stresses during the development of P. massoniana. The network diameter, modularity, average degree, and average path length of the abundant bacterial co-occurrence network were lower than those of the rare groups. However, the abundant bacteria exhibited a clustering coefficient and graph density than the rare bacteria (Table 2). These differences in network topology characteristics indicated that rare taxa have a greater network scale and complexity and more sensitivity to the environment than abundant taxa. However, there was a higher degree of aggregation of abundant bacterial taxa, which may contribute to buffer the environmental stress.

3.4. Variations in the Potential Functions of Abundant and Rare Bacterial Taxa

The variations in the functional OTU richness with P. massoniana development in the abundant and rare subcommunities were explored by PCA (Figure 4). FAPROTAX analysis found that the numbers of abundant and rare bacteria potential functions were 31 and 38, respectively (Supplementary Table S1). The main functions of abundant bacteria in young stands (i.e., 13-yr and 25-yr-old) were promoting nitrogen supply, while those in old stands (i.e., 38-yr and 58-yr-old) were to promote litter decomposition. However, the potential functions of the rare bacterial community were more diverse than the abundant taxa along the development of P. massoniana. From the results of rare bacterial PCA, PC1 represented the rare bacteria potential functions as an increase in both nitrogen supply and litter decomposition, while PC2 represented an increase in litter decomposition capacity but decrease in nitrogen supply capacity.

3.5. Associations between Soil Physicochemical Properties and Bacterial Functions

The Mantel test showed the relationships between the soil physicochemical properties and enzyme activities with the diversity, and structure of bacteria (Figure 5). Soil nutrient content and enzyme activity have stronger effects on abundant than rare bacterial communities. For the abundant taxa, soil pH, nitrogen pool (i.e., MBN, NH4+, NAlkali), and enzyme activities related to nitrogen conversion were the dominant factors associated with the changes in diversity, and structure stand ages. However, more soil variables influenced the changes in rare bacterial communities. Specifically, the soil water content, AP concentration, and sucrase activity were the dominant factors in determining rare bacterial community diversity. Soil pH, nitrogen pool (i.e., MBN, NH4+, NO3−, NAlkali), and sucrase activity were the dominant factors in determining the rare bacterial community structure.

4. Discussion

Plantation forest development usually implies a decline in soil microbial diversity, and net primary productivity due to nutrient supply deficiencies resulting from limited rates of soil organic matter decomposition and mineralization [6,34]. This process may be reinforced by the uneven bacterial community in a given plantation forest soil ecosystem [7,14]. Therefore, elucidating the feedback and response mechanisms of rare and abundant bacterial communities to plantation development is essential for the intensive management of plantation forests in the future.
The diversity of abundant and rare bacterial communities responds in significantly different patterns to the plantation forest development. In this study, rare bacterial communities exhibited higher richness and α-diversity (Shannon) than the abundant taxa during P. massoniana development (Figure 1). This result is consistent with previous studies [32,35] indicating that rare communities are the main contributors to the alpha diversity of the soil bacterial community. Logares et al. [36] suggest that the metabolic spectrum diversity of rare bacteria allows them to respond rapidly to variable environments and become a source of soil bacterial community diversity. We found that the soil bacterial diversity was higher in the young stands (i.e., 13-yr and 25-yr-old) than in the old stands (i.e., 38-yr and 58-yr-old). This can be attributable to the recombination of soil nutrients (especially for N, P, and K) and soil enzymes across the development of plantation [10,34]. Abundant and diverse forest legacy (e.g., litter and dead roots) can flourish the bacteria communities for decades after afforestation [37,38]. However, due to the accumulation of resistant decomposition substances such as lignin and rosin in litter during the development of P. massoniana, these substances could inhibit the mineralization and release of nutrients such as soil C, N, and P [39,40]. Instead, a nutrient turnover efficiency and higher mineralization capacity at young stands may favor microbial proliferation, thus there was higher bacterial diversity in young stands. However, compared to the abundant taxa, rare bacterial community diversity showed insignificant changes across four stand ages. This may also be related to the higher diversity and intrinsic growth rates of rare bacterial communities, which allows them to respond rapidly to environmental changes without a loss of diversity [32,41]. However, phenolics (e.g., tannins) produced during the decomposition of pine forest litter can form many insoluble complexes with proteins, metal ions, or biopolymers, which can be toxic to microorganisms and promote fluctuating changes in abundant bacterial diversity [42]. As a result, both abundant and rare bacterial communities were inconsistent across the plantation development process [43,44,45]. These results suggest that future microbial diversity studies should focus on the differential contributions of diverse taxonomic microorganisms to community diversity, rather than a simple global diversity.
Our study observed that abundant and rare taxa dominant phylum included Acidobacteria, Proteobacteria, Chloroflexi, Actinobacteria, Planctomycetes, Verrucomicrobia, Gemmatimonadetes, Firmicutes, and Bacteroidetes. However, the relative abundance varied significantly among the different taxa and forest stand ages at the same phylum. One reason for this may be that these bacterial phyla have stronger adaptability to environmental changes, but such capacity varies with species [14,19]. For example, Proteobacteria, Firmicutes, and Bacteroidetes are considered to belong to the copiotrophs, they were more abundant in nutrient rich stand ages (i.e., 13-yr and 25-yr-old). While Acidobacteria, Chloroflexi, Actinobacteria, Verrucomicrobia, Gemmatimonadetes belong to the oligotrophs, they were more active in nutrient limited stand ages (i.e., 38-yr and 58-yr-old) [4]. Although it is naive to simply classify a given bacterial phylum as a copiotrophic or oligotrophic type, since both plant communities and climatic conditions may contribute to changes in genera under the same phylum. More research is required in the future to determine a more precise classification of copiotrophic or oligotrophic types of microorganisms across different habitats. In addition, such a simple classification may also obscure the contribution of different sub-communities to ecological properties of the bacterial community. For example, the part of Proteobacteria belonging to the copiotrophs in the rare taxa with the highest abundance in the 25-yr-old stand, while the part belonging to the abundant taxa groups was the most abundant in the 38-yr-old stand. We also found that the abundance of Nitrospira for abundant taxa showed consistent trends with soil available N, P, and K during the development of P. massoniana (Table 1). This may suggest that the functional bacteria species could activate the legacy nutrients after clearcutting afforestation, but such an effect was slowly attenuated after the rapid growth period (i.e., young stands) of P. massoniana [26,38]. In addition, the abundance of the specialized parasitic pathogenic phylum (i.e., Chlamydiae) in rare taxa increased with forest age, which may also be the main reason for the decrease in bacterial diversity as the monoculture plant filtering effect may prefer to retain the bacteria species that better adapts to local or even regional soil environment change [7,43]. However, the abundance of Chlamydiae in rare taxa increased with the stand age, whether this is due to a strong adaptive ability or a biological disease controller in conifer remains to be further investigated.
Co-occurrence network analysis has been applied to reveal the microbial interactions and has received much attention in recent years [20,22]. In this study, we constructed the symbiotic networks for the abundant and rare taxa in response to the development of P. massoniana. It was shown that positive correlations dominated the co-occurrence networks of rare and abundant bacteria. The positive associations dominated within the bacterial communities, which indicated that cooperation might contribute to the resilience of the abundant or rare bacterial communities during the development of P. massoniana. Because the metabolic functions of species that assemble to coexist in the same habitat tend to be in a similar manner, which results in the functional redundancy of species to buffer the survival pressure from unfavorable environments [22,44]. However, the rare taxa had higher modularity and a larger network size than the abundant taxa but a lower clustering coefficient (Figure 4). This result may be attributed to the following reasons: (i) a higher diversity of rare bacterial species may favor more mutualistic symbiosis relationships in coniferous plantation soils [20,44]; and (ii) the environmental stresses generated by the developmental processes of planted forests may force most of the abundant bacteria to cooperate, but the competitive exclusion effect results in a modular symbiotic network [6,22]. The proportion of soil fungi (e.g., ectomycorrhizal fungi) also increases with the maturation process of coniferous plantations, and the effects of fungi on bacteria such as nutrient competition or predation may force bacteria to form symbiotic mutualisms in response to this pressure [45,46]. However, since abundant bacterial communities are more resistant to stress than rare bacterial communities, the abundant bacterial co-occurrence network has a small scale but is tightly connected, while the rare bacterial co-occurrence network has a large scale but lower modularity.
Microbial communities are the main drivers of soil ecosystem functions, especially in nutrient cycling [15]. According to the results of FAPROTAX and PCA, we found that the rare and abundant bacterial potential functions were dominated by the promotion of N supply at young stands (i.e., 13-yr and 25-yr-old) and by the promotion of litter decomposition at old stands (i.e., 38-yr and 58-yr-old). This can be attributed to changes in the demand for N during the growth of P. massoniana. The demand for soil N could result in a higher abundance of functional bacteria which is related to N transformation (e.g., Nitrospirae) in young stands [47,48]. With the pine maturation, however, the depletion of legacy nutrients forces P. massoniana to select more special decomposing and mineralization bacteria, which in turn compensate for the soil nutrient supply deficits. We also found that the rare bacterial communities mediated more functions that shifted from sulfur respiration, chitinolysis, and aromatic compound degradation in the 25-yr-old stand to nitrate respiration and anaerobic ammonia oxidation in the 38-yr and 58-yr-old stands (Figure 3). These potential functional changes may be caused by the turnover of lignin and aromatic compounds from the litter of P. massoniana at different stand ages [38,49]. These changes were also in parallel within the N, P, and K contents and enzyme activities from the young stands (i.e., 13-yr and 25-yr-old) to old stands (i.e., 38-yr and 58-yr-old) (Table 1). Litter accumulates with increasing stand age, which creates a micro-anaerobic environment and may be the reason for the aerobic potential bacterial community functions such as aerobic nitrite oxidation, aerobic ammonia oxidation, and nitrification decreased with an increase in the stand age, while an increase in the anaerobic bacterial community functions such as fermentation, chemoheterotrophy, and anammox (Figure 3). For example, Fe-OM produced by the iron respiration process would limit litter decomposition during the development of plantations [10,50]. In addition, there are more function species of rare than abundant taxa, and may support the demand for substances such as proteins and amino acids in the young stand (i.e., 13-yr and 25-yr-old) [10,42,51]. The function redundancy of the rare taxa bacterial community could also offset the regional ecosystem function degradation caused by monoculture pine plantations [22,35]. Therefore, the abundant taxa bacterial communities dominate and maintain the main functions, while the rare taxa bacterial communities may be the potential functional pool during the P. massoniana development.
Advances in high-throughput sequencing technologies have provided great convenience in revealing the ecological functions of soil microorganisms, but previous studies often neglected the differences in the responses of diverse subcommunities to the soil environmental variables [36]. Characterizing the response of abundant and rare bacterial communities to soil physicochemical properties is essential for understanding the microbial community dynamics and ecosystem functional characteristics. The response of rare soil and abundant bacterial community diversity and structure to soil variables was distinct [41,46]. In this study, we found that changes in soil pH and N content were significantly correlated with the diversity and structure of rare bacterial communities during the development of P. massoniana. The soil pH decreased with increasing coniferous forest age, which in turn affects the soil bacterial community dynamics [2,52,53]. In addition, as the process of NH4+ to amino acids in microorganisms requires less energy than that of NO3−, NH4+ was the dominant factor affecting the structure and diversity of the abundant bacterial community [48,54,55]. However, compared to the abundant bacteria, rare bacterial communities were affected by more soil variables such as soil water, available phosphorus, N pool, and so on (Figure 5). The phylogenetic diversity of rare bacteria implies a diversity of metabolic types, which may result in a higher diversity of soil variables that regulate the stability or variability of rare bacterial communities than the abundant groups [22]. These differences in abundant and rare taxa result in significantly different responses to soil variables and enzyme activities, which may in turn directly or indirectly alter their mediated functions. Therefore, more attention should be paid to the changes in soil bacterial subcommunities in the study of intensively managed plantation forest ecosystems.

5. Conclusions

In this study, we observed that the abundant and rare bacteria community diversity and composition responded differently to the development of the plantation forest of P. massoniana. Bacterial diversity decreased with the development of the P. massoniana plantation forest. Both abundant and rare bacterial co-occurrence networks were dominated by significant positive correlations. However, the rare bacterial network scale, average degree, and clustering coefficient were higher than those of the abundant bacteria. Soil pH and N pool were important factors in regulating the community diversity of both abundant and rare bacteria, but rare bacterial community dynamics were regulated by a broader range of soil variables. Potential bacterial function predictions indicated that rare bacterial communities mediated more potential functional enrichment, and they seemed to be a functional pool during the development of P. massoniana. Therefore, rare bacteria with diverse phylogeny are the soil bacterial diversity pool, and they may be more important than abundant bacteria in the soil nutrient support functions. We suggest that future studies should focus on the response of different subcommunities to changes in the plantation forest community.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f13111904/s1, Table S1: OTUs correspondents to ecological functions.

Author Contributions

Conceptualization, Y.Z.; Methodology, H.Z.; Investigation, H.Z.; Data curation, Q.C.; Formal analysis, Q.C.; Writing-original draft preparation, Q.C.; Writing-review and editing, Q.C., Y.Z. and Y.B.; Supervision, Y.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the National Natural Science Foundation of China (Grant NO. 32260375), The first-class discipline construction project in Guizhou Province (GNYL (2017) 007), the 100 High-Level Innovating Project (Grant No. QKHRC-2015-4022), Postgraduate Education Innovation Program in Guizhou Province [YJSKYJJ (2021)049], and the Plateau Mountain National long-term Pinus massoniana Scientific Research Base (2013132093).

Data Availability Statement

The sequencing raw reads were deposited into the NCBI Sequence Read Archive (SRA) database https://www.ncbi.nlm.nih.gov/sra/ (accessed on 18 September 2018), Accession Number: PRJNA491760.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. OTU richness and Shannon index of abundant and rare bacterial community (A,B). The relative abundance changes in the top 10 abundant phyla in the abundant and rare taxa across different stand ages (C,D). Columns are the mean ± SE (standard error). The same lowercase letters indicate that the same taxa have no difference across P. massoniana stands of different ages.
Figure 1. OTU richness and Shannon index of abundant and rare bacterial community (A,B). The relative abundance changes in the top 10 abundant phyla in the abundant and rare taxa across different stand ages (C,D). Columns are the mean ± SE (standard error). The same lowercase letters indicate that the same taxa have no difference across P. massoniana stands of different ages.
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Figure 2. Principal coordinate analysis (PCoA) showing the composition of bacterial communities of abundant and rare taxa across P. massoniana stands of different ages.
Figure 2. Principal coordinate analysis (PCoA) showing the composition of bacterial communities of abundant and rare taxa across P. massoniana stands of different ages.
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Figure 3. Co-occurrence networks of abundant and rare taxa. The size of the node represents the degree of OTUs. The dotted line between the OTUs represents the positive (red) correlation and negative (green) correlations.
Figure 3. Co-occurrence networks of abundant and rare taxa. The size of the node represents the degree of OTUs. The dotted line between the OTUs represents the positive (red) correlation and negative (green) correlations.
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Figure 4. Principal component analysis of the functional OTU richness of abundant and rare bacterial taxa during P. massoniana development.
Figure 4. Principal component analysis of the functional OTU richness of abundant and rare bacterial taxa during P. massoniana development.
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Figure 5. Partial Mantel correlation test between the soil physicochemical properties and bacterial α−diversity and composition for abundant and rare bacterial taxa. Community diversity includes OTU richness, the Shannon index, and the Pilou index. Community structure was expressed as PC1 and PC2 of the PCoA results of abundant and rare bacterial taxa. The width of the edges represents the R2 of the Mantel test. The colors represent the p-values, which were based on 999 permutation tests. SW: soil water content; MBC: microbial biomass carbon; MBN: microbial biomass nitrogen; SOC: soil organic carbon; TN: total nitrogen; N alkali: alkali nitrogen; TP: total phosphorus; AP: available phosphorus; TK: total potassium; AK: available potassium; NR: nitrite reductase.
Figure 5. Partial Mantel correlation test between the soil physicochemical properties and bacterial α−diversity and composition for abundant and rare bacterial taxa. Community diversity includes OTU richness, the Shannon index, and the Pilou index. Community structure was expressed as PC1 and PC2 of the PCoA results of abundant and rare bacterial taxa. The width of the edges represents the R2 of the Mantel test. The colors represent the p-values, which were based on 999 permutation tests. SW: soil water content; MBC: microbial biomass carbon; MBN: microbial biomass nitrogen; SOC: soil organic carbon; TN: total nitrogen; N alkali: alkali nitrogen; TP: total phosphorus; AP: available phosphorus; TK: total potassium; AK: available potassium; NR: nitrite reductase.
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Table
Table 1. Edaphic properties and enzyme activities according to four stand ages (Mean ± SE). Significance levels: ** p < 0.01, * p < 0.05.
Table 1. Edaphic properties and enzyme activities according to four stand ages (Mean ± SE). Significance levels: ** p < 0.01, * p < 0.05.
13-yr25-yr38-yr58-yrF Value
MBC (mg kg−1)334.17 ± 12.97 a326 ± 11.61 a207.94 ± 1.65 b253.05 ± 10.82 b21.58 **
MBN (mg kg−1)73.22 ± 4.5 b116.81 ± 5.7 a35.54 ± 2.42 c33.13 ± 2.98 c100 **
Nalkali (mg kg−1)135.09 ± 10.92 b235.12 ± 21.27 a102.79 ± 6.31 b136.88 ± 16.93 b7.89 **
TP (g kg−1)0.42 ± 0.03 a0.3 ± 0.01 b0.13 ± 0.01 c0.12 ± 0.01 c60.87 **
AP (mg kg−1)2.33 ± 0.2 a1.83 ± 0.14 b1.79 ± 0.1 b2.24 ± 0.05 ab4.07
TK (g kg−1)2.55 ± 0.12 a2.09 ± 0.22 a1.72 ± 0.42 a1.38 ± 0.32 a1.23
AK (mg kg−1)54.05 ± 4.48 ab68.79 ± 8.25 a43.09 ± 5.77 b28.32 ± 4.58 b5.67 *
Nitrite reductase (μg g−1)4.99 ± 0.58 b11.18 ± 1.04 a7.76 ± 2.48 a3.98 ± 0.02 b26.26 **
Urease (mg g−1)0.65 ± 0.09 b0.99 ± 0.06 a0.13 ± 0.02 c0.19 ± 0.04 c57.88 **
Invertase (mg g−1)28.2 ± 2.2 a18.25 ± 1.85 b19.64 ± 0.38 b23.4 ± 1.08 b7.53 *
MBC: microbial biomass carbon; MBN: microbial biomass nitrogen; Nalkali: alkali-hydrolyzable nitrogen; TP: total phosphorus; AP: available phosphorus; TK: total potassium; AK: available potassium. Different lowercase letters indicate significant differences between different stand ages (p < 0.05).
Table
Table 2. Topological properties of co-occurrence networks of the abundant and rare bacteria.
Table 2. Topological properties of co-occurrence networks of the abundant and rare bacteria.
ModularityClustering CoefficientAverage Path LengthNetwork DiameterGraph DensityAverage Degree
Abundant0.410.813.1712.090.0563.81
Rare0.580.615.85160.03186.45
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Cao, Q.; Zhou, Y.; Zhao, H.; Bai, Y. Inconsistent Response of Abundant and Rare Bacterial Communities to the Developmental Chronosequence of Pinus massoniana. Forests 2022, 13, 1904. https://doi.org/10.3390/f13111904

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Cao Q, Zhou Y, Zhao H, Bai Y. Inconsistent Response of Abundant and Rare Bacterial Communities to the Developmental Chronosequence of Pinus massoniana. Forests. 2022; 13(11):1904. https://doi.org/10.3390/f13111904

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Cao, Qianbin, Yunchao Zhou, Hui Zhao, and Yunxing Bai. 2022. "Inconsistent Response of Abundant and Rare Bacterial Communities to the Developmental Chronosequence of Pinus massoniana" Forests 13, no. 11: 1904. https://doi.org/10.3390/f13111904

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