The bacterial community inhabiting temperate deciduous forests is vertically stratified and undergoes seasonal dynamics
Introduction
Temperate deciduous forests represent one of the most important carbon (C) sinks in Europe, Asia and Northern America and contribute to the health of the planet (Janssens et al., 2003). The flux of C into these ecosystems is mainly mediated by the photosynthetic fixation of CO2 by broadleaved trees, its allocation belowground via tree roots in the form of root exudates and root litter and the accumulation of the aboveground litter on the forest floor due to yearly seasonal litterfall. This pool of C-rich organic matter (OM) is used as a carbon and energy source by a diverse community of microorganisms, responsible for its transformation and mineralization throughout the year (Uroz et al., 2011, Rasche et al., 2011, Voříšková et al., 2014). Microbial communities thus play a critical role in soil biogeochemical processes, as the main drivers of C efflux from the ecosystem and its transformation, resulting in the formation of a forest soil profile, one of the most diverse habitats on Earth (Roesch et al., 2007). The yearly input of litter and the ongoing decomposition process in forests result in three distinct topsoil compartments: the litter, the organic (or humic) horizon and the mineral soil horizon. This vertical stratification is characterized by a decrease in the content and quality of OM with soil depth, which is accompanied by changes in the activity of extracellular enzymes and in the size and composition of the microbial community (Sinsabaugh et al., 2002, Šnajdr et al., 2008a).
In addition to the organic matter in the soil, microbial activity is also influenced by environmental factors, with the variations in temperature and moisture across different seasons being the most notable (Brockett et al., 2012). In a temperate forest, temperature variation due to seasonality directly influences C fluxes in the ecosystem (Baldrian et al., 2013). Most importantly, the photosynthetic production of plants is limited to the vegetation period. As a consequence, the increasing rate of photosynthesis during the spring and summer is associated with the deposition of easily decomposable compounds, such as amino acids, sugars and organic acids, into plant roots and the deeper soil horizons either directly or in a process mediated by root-associated mycorrhizal fungi (Ekblad and Högberg, 2001). The annual period of litterfall restricted to autumn and early winter leads to the seasonal accumulation of large amounts of nutrients on the soil surface. The continuous decomposition of litter results in gradual changes in its quality until the next litterfall (Šnajdr et al., 2011, Baldrian et al., 2013). Microbial communities are subject to these profound changes in nutrient content and composition during the year, which results in seasonal changes in their abundance and activity (Kaiser et al., 2010; Voříšková et al., 2014). Importantly, the understanding of the seasonal dynamics of microbial communities is necessary for the prediction of the future response of temperate deciduous forests to global climate change and its effects on the C balance in the ecosystem (Schindlbacher et al., 2012, Rousk et al., 2012).
Several previous studies reported that seasonality may affect the structure of microbial communities and the functional properties of soil microorganisms in the temperate forest, suggesting that microbial dynamics is mainly influenced by changing temperature, moisture and nutrient availability (Collignon et al., 2011, Chemidlin Prevost-Boure, 2011, Rasche et al., 2011, Koranda et al., 2013). However, the resolution of most of this work was limited by the use of methods based on DNA fingerprinting or qPCR, which are insufficient for the characterization of the community composition (Osborn et al., 2000, Zhang et al., 2008). High-throughput DNA pyrosequencing provides more detailed information on microbial communities inhabiting soils (Roesch et al., 2007) and has been successfully used to explore the ecology and diversity of soil microorganisms in a wide variety of types of ecosystems (Lauber et al., 2009, Eilers et al., 2012, Uroz et al., 2013, Williams et al., 2013). Recently, Voříšková et al. (2014) applied pyrosequencing for the in-depth description of the seasonal development of the structure and functioning of fungal communities and demonstrated that the fungal abundance and community composition undergoes seasonal changes. The effects of seasonality on bacterial communities using pyrosequencing was highlighted by Kuffner et al. (2012), who found no substantial differences in a mountainous forest between these communities across the seasons. Unfortunately, that study only compared summer and was performed in a forest with prevailing evergreen coniferous trees where the litter input is not seasonally restricted. Moreover, the limitation of the study to soil makes any inferences on carbon balance difficult because the bulk of the organic matter loss and microbial activity occurs in litter (Šnajdr et al., 2011, Šnajdr et al., 2008a). The analysis of a deciduous forest ecosystem considering both litter and soil are unavailable.
The aim of this work was to fill this knowledge gap by describing the bacterial community living in the litter and upper soil and determining how it changes throughout the year. We hypothesized that phenomena such as litter input, temperature and moisture variation and the seasonal pattern of C rhizodeposition would affect the bacterial community composition across the year. The data describing the bacterial community composition were obtained from the same study that analyzed the seasonality of fungi (Voříšková et al., 2014). That study showed that the fungal community is stratified in the soil profile and its composition in litter undergoes profound seasonal changes as a consequence of changing litter chemistry. In contrast, despite the fact that root-associated fungi dominated deeper soil horizons where they could have theoretically responded to changes in root exudation, the seasonal changes in fungal community composition were minor. Based on that observation, we suggest that the seasonality of bacterial communities is horizon specific and most pronounced in the litter because there are many bacterial taxa that are involved in decomposition in forest ecosystems (Štursová et al., 2012). The parallel exploration of the fungal and bacterial community dynamics should also complete the picture of microbial response to ecosystem seasonality and reveal possible differences among these ecophysiologically distinct groups of microorganisms (Boer et al., 2005).
Section snippets
Site description and sample collection
The experimental study site was situated in a sessile oak (Quercus petraea) forest in the Xaverovský Háj Natural Reserve in the Czech Republic (50°5′38″N, 14°36′48″E). Soil and litter chemistry and decomposition processes have been studied in the area previously (Šnajdr et al., 2008a, Šnajdr et al., 2011, Baldrian et al., 2013), as well as the structure and functioning of fungal communities associated with litter and soil (Voříšková and Baldrian, 2013, Voříšková et al., 2014). The soil was an
Soil characteristics and pyrosequencing dataset analysis
The data obtained in a previous study (Voříšková et al., 2014) revealed that the physicochemical properties of forest soil change significantly with the soil depth. In particular, the content of organic matter, N content, pH and activity of extracellular enzymes all decreased with depth, while the soil moisture content increased. Seasonality also affected soil properties during the year, resulting in significant differences of soil chemistry and enzyme activity among seasons (Fig. S1).
In total,
Discussion
Bacterial communities inhabiting the forest soil are important players in geochemical cycles and the recycling of organic matter, thus playing an essential role in C cycle in these ecosystems (Štursová et al., 2012). Our results showed that forest soil was dominated by the same major groups (Acidobacteria, Proteobacteria, Actinobacteria, and Bacteroidetes) reported from acidic soils of various biomes (Lauber et al., 2009, Peralta et al., 2013). Previous studies of the diversity of bacterial
Conclusions
This study shows that for bacteria, as for fungi, soil communities in a deciduous forest differ in their composition among litter, organic soil and mineral soil. In contrast to fungi, bacterial communities exhibit significant horizon-specific seasonal changes. While the annual changes in litter quality seem to drive the composition of the bacterial community in litter, the specific composition of the summer bacterial community in the mineral soil indicates that the seasonal differences in the
Acknowledgments
This work was supported by the Ministry of Education, Youth and Sports of the Czech Republic projects CZ.1.07/2.3.00/30.0003, LD12048 and LD12050, and BIOCEV – Biotechnology and Biomedicine Centre of the Academy of Sciences and Charles University No. CZ.1.05/1.1.00/02.0109 from the European Regional Development Fund in the Czech Republic, and by the Research Concept of the Institute of Microbiology ASCR (RVO61388971).
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