Temperature is one of the most important factors influencing soil organic matter decomposition and microbial communities. For example, temperature significantly affects the soil microbial phospholipid fatty acid composition associated with straw decomposition at the early stage (Zhou et al., 2016). Bacterial abundance increases in conditions of elevated temperature and CO2 concentration (Castro et al., 2010). The complex responses of bacterial composition and diversity of bamboo soils across altitudinal gradients have been suggested to result from interactions with multiple factors, including temperature (Lin et al., 2015).

In Taiwan, moso bamboo (Phyllostachys pubescens) is an important versatile forest resource that is widely used for food, construction, and as a furniture material. It is distributed from low- to high-mountain regions at approximately 1800 m above sea level (a.s.l.). Management practices for increasing bamboo production, including regular removal of understory vegetation, tillage, and fertilizer application, can increase the soil CO2 efflux (Liu et al., 2011) and water-soluble organic N concentration (Wu et al., 2010). However, these management practices can lower the microbial functional diversity (Xu et al., 2008). Considering the effects of bamboo plantations on soil properties and microbial communities, it is worth elucidating the changes in bamboo soil bacterial communities under environmental changes.

Our previous study revealed that bamboo invasion could increase bacterial diversity and alter the bacterial structure of adjacent cedar forest soils (Lin et al., 2014). Soil bacterial diversity in bamboo plantations showed a hump-backed trend, with less diversity at low and high elevations, and maximum diversity at middle elevations, and community structure formed different clusters at different elevations (Lin et al., 2015). Our parallel study showed that invasion of bamboo into adjacent forest soils increased humification of soil organic matter (SOM) (Wang et al., 2016b). In addition, changes in the SOM pool and the rate of humification with elevation were primarily affected by changes in climatic conditions along the elevation gradient in the bamboo plantations (Wang et al., 2016a). However, it is not known whether bamboo soil bacterial groups respond to temperature changes.

Soil bacterial communities include different phylotypes that likely represent different functional groups, and their relative abundances are affected by carbon (C) availability. For example, some members of Proteobacteria are considered copiotrophs, and their relative abundances appear to be higher in C-rich environments. In contrast, oligotrophs (e.g., Acidobacteria) can live in stressful environmental conditions (Fierer et al., 2007). However, little is known about how these two groups respond to the environmental temperature changes. Here, we hypothesized that the temperature changes would alter the structure and diversity of soil bacterial communities at different elevations, and that bacterial taxa, including copiotrophic and oligotrophic groups, would have distinct responses to altered nutrient availability caused by temperature changes. To test these hypotheses, soil communities sampled at bamboo plantations at three elevations were incubated at different temperatures and investigated by using the barcoded pyrosequencing technique. The objectives of this study were to elucidate (1) changes in soil organic carbon, nitrogen, and respiration at elevation gradients and at different incubation temperatures, (2) differences in bacterial structure and diversity under different incubation temperatures and periods, and (3) changes in the abundances of different phylogenetic groups at different incubation temperatures.

The present study revealed that the SOC content was higher at high incubation temperature and decreased with increasing elevation after long incubation. The soil respiration CO2-C rate was greater at higher elevation. Similarly, a previous study in tundra soils using different incubation temperatures reported higher respiration rate at high temperatures (Stark et al., 2015). Incubation at increasing temperatures enhanced the soil microbial activity and led to an increase in soil respiration in forest mesocosms (Lin et al., 2001). In our study, the respiration rate decreased after long incubation. This could be due to the exhaustion of labile compounds after microbial decomposition (Zhou et al., 2016). The decrease in bacterial diversity at high elevation and high incubation temperature, calculated from abundance data of the phylogenetic groups, could also be the result of nutrient exhaustion after long incubation. In addition, the correlation between soil respiration and bacterial structure in the soil samples under incubation at 35 ∘C suggests the adaption and high activity of bacterial communities at higher temperature.

In d0 samples, which represent the original composition of the bamboo soils, the bacterial diversity was higher in the 1800 m soils, followed by the 600 and 1200 m soils. Communities with higher diversity are reportedly more resistant to environmental changes (Loreau and de Mazancourt, 2013). In a study by Ren et al. (2015) in rice paddies, the diverse soil communities were more resistant to elevated CO2 and temperature than the less diverse foliar bacterial communities. The increasing concentration of recalcitrant C with increasing elevation (Wang et al., 2016a) could be helpful in providing more carbon resources to the community at high elevation. Together, these findings indicate that bamboo soil bacterial communities with higher diversity could be more capable of maintaining soil community and function when exposed to climatic changes and subjected to management at high elevation (1800 m).

The bacterial community structure varied over different incubation periods and temperatures. Based on the abundance data of phylogenetic groups, the communities at the three elevations formed different clusters as compared to the results of our previous study (Lin et al., 2015). The different soil bacterial structures at different elevations can be explained by differences in soil management. The effects of management practices on soil microbial community can persist over time (Keiser et al., 2011). Recently, bamboo shoot harvest and timber production has moved from about 600 to 1200 m in the study area. Soils at different elevation have distinct soil SOC and SON contents, which could result in different forces to alter bacterial communities. Incubation temperature also had an effect on community structure. Warming in the experimental field in a previous study in the Arctic environment caused a significant increase in the abundance of fungi and bacteria (Yergeau et al., 2012). The quantity of SOC and CO2 flux has been shown to increase under warming conditions (Zhang et al., 2005; Zhou et al., 2011). Increasing temperature increased relative bacterial growth in arable soils from southern Sweden (Bárcenas-Moreno et al., 2009) and, particularly, the abundance of genes involved in labile carbon degradation in a tall-grass prairie ecosystem in central Oklahoma, USA (Zhou et al., 2011), and led to C loss. In the present study, the shifts in bacterial communities at three elevations could reflect differences in nutrient availability, including SOC and SON, and bacterial activity under different incubation temperatures and at distinct time points during incubation.

Bacterial community structure under incubation at 35 ∘C was affected by temperature, while under incubation at 15 and 20 ∘C it correlated with incubation time (Fig. 7). Warming has been shown to change the bacterial structure of alpine meadow soils (Xiong et al., 2014) and to cause thermal-adaption functional shift of microbial communities (Rousk et al., 2012). Recent studies have observed changes in temperature sensitivity of microbial communities along incubation time. Shifts in microbial communities in response to warming occur after a few years (Yergeau et al., 2012) or even only a few months (Xiong et al., 2014). However, some studies revealed no significant community changes over time owing to warming (Allison et al., 2010; Zhou et al., 2011). The present work revealed community structure differences after incubation for only about 4 months, suggesting that the bacterial communities in bamboo soils at elevation are highly sensitive to temperature changes, even though they faced a relatively short-time warming condition.

The responses of phylogenetic abundances to temperature differed. As for Acidobacteria, the abundance generally decreased with increasing temperature. This is in accordance with previous studies showing decreases in the relative abundance of Acidobacteria in warming soils (Xiong et al., 2014; Yergeau et al., 2012). Acidobacteria are known as slow-growing (oligotrophic) bacteria that prefer low nutrient availability (Fierer et al., 2007) and possess high maximum growth efficiency (Roller and Schmidt, 2015). Warming conditions in the soil could increase substrate availability and might favor fast-growing (copiotrophic) microorganisms, which are more sensitive to nutrient availability (Männisto et al., 2016). Thus, the decreases in the abundance of Acidobacteria could reflect their interactions with copiotrophic species. The abundance of Acidobacteria could also be limited by high temperatures (Stark et al., 2015).

Under increased temperature, some phyla in our study responded differently from previous studies. Increasing α-Proteobacteria abundance has been observed in short warming conditions (Xiong et al., 2014) and in a range of Antarctic environments (Yergeau et al., 2012). α-Proteobacteria are mostly fast-growing (copiotrophic) bacteria and are known to be positively correlated with soil available C pools (Nemergut et al., 2010). The decreases in the abundance of α-Proteobacteria in the present study could reflect the decrease in SOC content, which was exhausted by soil respiration CO2-C after incubation. Bradyrhizobium of α-Proteobacteria at 1800 m increased at all three incubation temperatures. This genus includes species capable of nitrogen fixation and may significantly contribute to soil function (Yarwood et al., 2009). The increase in their abundance might explain the elevated SON. Moreover, these bacteria are plant-growth-promoting bacteria, stimulating plant growth by fixing N2, increasing the availability of nutrients in the rhizosphere, positively influencing root growth and morphology, and promoting other beneficial plant–microbe symbioses (Vessey, 2003). Their response to incubation temperatures indicates their potential roles in bamboo growth and responses to application of fertilizers under climatic change.

The increase in abundance of γ-Proteobacteria after incubation in our study differed from that in the soil community sampled at elevated soil temperature. γ-Proteobacteria showed a lower relative abundance under elevated temperature than in the ambient temperature control (Ren et al., 2015). Within β-Proteobacteria, the abundant genus Burkholderia is nutritionally versatile and is commonly found in rhizosphere soils. Their functional diversity, including nitrogen fixation and plant growth promotion (Coenye and Vandamme, 2003), could help maintain soil community stability. In addition, Actinobacteria and Bacteroidetes showed variable responses at different temperatures. These phyla also prefer nutrient-rich environments (Nemergut et al., 2010). Differences in vegetation and litter quality among the study sites might explain this variation. Actinobacteria are involved in the organic matter degradation. Under climatic changes, managements of bamboo forests need to consider the responses of Actinobacteria to temperature, especially that in N fertilizers, since the abundance of this phylum was positively affected by N fertilization treatments (Zhou et al., 2015). The Mucilaginibacter species of Bacteroidetes are capable of degrading polysaccharides (Pankratov et al., 2007); thus, the increase in their abundance can be explained by the increase in plant residues in the soil. A previous study suggested the relationship of elevation and temperature with the decomposition of recalcitrant C (Wang et al., 2016a). After decomposition of labile C, the availability of recalcitrant C can strongly affect the community. Moreover, based on a literature survey by Ho et al. (2017), there is little consistency in oligotrophic and copiotrophic phyla of bacterial communities. The microorganisms can display a variety of metabolic characteristics and adjust between high and low substrate use efficiency to adapt to environmental changes. Therefore, shifts in the relative abundances of bacterial taxa may not necessarily indicate their life strategies as an oligotroph or copiotroph but might just reveal the response of a community to such local factors (Ho et al., 2017). Further study, including more comprehensive temperature gradients and more detailed time-course analysis, will be necessary to elucidate the exact influences of temperature on soil communities.

Acidobacteria and α-Proteobacteria, which comprised more than 10 % of the communities before incubation, tended to decrease after incubation. Groups with lower abundance before incubation, especially, γ-Proteobacteria, showed an increasing trend after incubation. These patterns were similar to those shown in communities of a rice paddy and desert soils (Wang et al., 2012; Ren et al., 2015), in which numerically dominant bacterial phyla/classes were reduced, while originally rare groups increased in relative abundance after exposure to environmental changes. These results suggest that shifts in bacterial populations facing environmental changes may follow predictable patterns.

Our results revealed that an increase in temperature could result in increased soil respiration CO2-C and consumption of SOC and SON contents, which directly or indirectly influence the bacterial diversity and structure of bamboo soils at different elevations. In addition, the different responses of bacterial groups to the temperature changes suggest the adaptation of soil communities to global-warming-related climatic changes. This study highlights the need for further research on the physiological and ecological roles of soil bacterial members, such as Acidobacteria, α- and γ-Proteobacteria, in response to climatic change in forest ecosystems.