Contrasting Euryarchaeota communities between upland and paddy soils exhibited similar pH-impacted biogeographic patterns
Introduction
Despite widespread occurrence and physiological diversity in terrestrial ecosystems, Euryarchaeota remain a largely less-explored Archaea phylum, which contain psychrophiles, thermophiles, mesophiles, halophiles and alkaliphiles, mostly with unresolved metabolic properties (Pesaro and Widmer, 2002; Poplawski et al., 2007). Euryarchaeota have been known to involve in greenhouse gas production, with methane as the end-product of the anaerobic respiration, and this biological process accounted for about 74% of the emitted atmospheric methane on Earth (Liu and Whitman, 2008). In addition to methanogenesis, Euryarchaeota were also found to be capable of oxidizing methane (Michaelis et al., 2002), fixing nitrogen (Raymond et al., 2004), reducing nitrate (Cabello et al., 2004), and metabolizing sulfur and iron (Edwards et al., 2000). Phylogenetic analyses of over 8,000 deposited archaeal rRNA gene sequences suggest that Euryarchaeota are the most diverse Archaea phylum, containing about 33 distinct phylogenetic groups (Schleper et al., 2005). However, currently available knowledge for the ecophysiological characteristics of Euryarchaeota primarily generated from the purely cultured strains and about 30 complete genome sequences deposited in databases, with most of them being distantly related to the mesophilic lineages, so there is still an incomplete understanding of the whole Euryarchaeota community (Barberan et al., 2011).
In addition to these culture-dependent studies, growing numbers of environmental ribosomal gene investigations have greatly expanded our view of Euryarchaeota with diverse and abundant uncultured lineages (Schleper et al., 2005). Euryarchaeota were frequently described and recovered in marine environments (DeLong, 1992), freshwater habitats (Auguet et al., 2010), hypersaline sediments (Hollister et al., 2010), paddy soils (Liesack et al., 2000), bovine rumen (Whitford et al., 2001), termite guts (Purdy, 2007), and anaerobic bioreactors (McHugh et al., 2003). Therefore, most of Euryarchaeota lineages were usually considered as strict anaerobes, and only sporadically reported in the well-aerated parts of forest, grassland and agricultural soil environments (Pesaro and Widmer, 2002; Poplawski et al., 2007). Compared with the intensively researched paddy soils, studies on Euryarchaeota in upland soil ecosystems are relatively less common, thus their potential function and community diversity were largely underestimated. For instance, the methanogens, being considered as strictly obligate anaerobic Euryarchaeota, were recently shown to diversify and successfully colonize in many types of aerated upland soils sampled globally (Angel et al., 2012). The methane production was activated when these upland soils were incubated under anoxic microcosms as slurry (Angel et al., 2012). In some other aerated surface upland soils, Euryarchaeota were reported with a high abundance, suggesting that certain Euryarchaeota groups were not strictly dependent on anoxic environments and might be tolerant to aerated conditions (Pesaro and Widmer, 2002; Bomberg and Timonen, 2007). But due to the methodological limitations employed in these studies, for example, Terminal Restriction Fragment Length Polymorphism (T-RFLP) and clone libraries which lacked phylogenetic or taxonomic resolution, our knowledge of these widely distributed Euryarchaeota in terrestrial environments still remains scarce.
With the advent of the barcoded pyrosequencing technology, we could now be able to survey the complex unculturable communities in a greater sequencing depth (Roesch et al., 2007). The superior advantages of next-generation sequencing have been exploited to elucidate the environmental distributions of soil-dwelling microbes across large-scale biogeographical regions (Jones et al., 2009; Lauber et al., 2009; Rousk et al., 2010). Some comprehensive surveys of terrestrial Archaea have provided valuable insights into the biogeographic patterns of the total Archaea community (Bates et al., 2011; Cao et al., 2012) or functional archaeal lineages (Gubry-Rangin et al., 2012; Pester et al., 2012), and showed great importance of environmental factors in structuring archaeal ecological niches. However, no studies have been carried out to directly compare the large-scale distribution patterns of Euryarchaeota across various terrestrial ecosystems. It remains not fully understood that whether aerated upland soils encompass contrasting or similar Euryarchaeota communities to anoxic terrestrial ecosystems (e.g. paddy soils), or whether these ecosystems exhibit similar soil variable-impacted distribution patterns.
The present study was designed to obtain a broad overview of the ecological characteristics of Euryarchaeota in 92 soil samples, collected from a wide variety of terrestrial ecosystems, including cropland, grassland, forest, tea orchard, and paddy soils. We used 454 barcoded pyrosequencing to generate archaeal 16S rRNA gene sequences, and compared the relative abundance, diversity, and taxonomic composition of the classified soil Euryarchaeota across different terrestrial biomes. We also tried to determine the influences of various edaphic factors on the biogeographic patterns of soil Euryarchaeota.
Section snippets
Soil sampling, physicochemical analyses and DNA extraction
In this study, totally 92 soil samples were collected across South and North China, as shown in Fig. S1 and Table S1. For each sample, 9 random cores were taken from the top 20-cm surface soils. Upland soil samples were composited and sieved through a 2.0 mm mesh to thoroughly homogenize. All paddy soils were collected during the rice-growing seasons, thus paddy fields were under flooded conditions. Paddy soil subsamples were pooled, and all the plant roots and stones were carefully removed.
Euryarchaeota community structures partitioned by terrestrial ecosystems
Across all the 92 samples examined, the barcoded pyrosequencing yielded 428,878 high-quality archaeal 16S rRNA gene sequences. Of these sequences, 96,534 (22.5% in average) could be classified into the Euryarchaeota phylum, and the other 77.5% was affiliated with the Crenarchaeota phylum. The similarity/dissimilarity of the Euryarchaeota communities across the 92 samples was measured by principal coordinate analyses (PCoA) of the pairwise Bray–Curtis dissimilarity matrices (Fig. 1). These
Contrasting Euryarchaeota community structures between upland and paddy soils
In this study, we presented a large-scale investigation into the Euryarchaeota community across several terrestrial ecosystems, typically representative in South and North China. By pyrosequencing the archaeal 16S rRNA gene, our results revealed that paddy soils exhibited contrasting Euryarchaeota community profiles from upland soil ecosystems at all taxonomic resolutions. No significant variations in Euryarchaeota community compositions were noticed within the different upland soil ecosystems.
Acknowledgments
This work was financially supported by the National Natural Science Foundation of China (41230857, 41090281, 41025004) and the Ministry of Science and Technology of China (2013CB956300). We gratefully acknowledge Prof. Linghao Li, Dr. Wenyan Han for access to the field trial stations, and Drs. Yong Zheng, Huaiying Yao, Qichun Zhang, Zili Yi, Xianjun Liu for assistance in soil sampling.
References (54)
- et al.
Insights into extreme thermoacidophily based on genome analysis of Picrophilus torridus and other thermoacidophilic archaea
Journal of Biotechnology
(2006) - et al.
Inhibition of anareobic digestion process: a review
Bioresource Technology
(2008) - et al.
Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils
Soil Biology and Biochemistry
(2012) - et al.
Microbiology of flooded rice paddies
FEMS Microbiology Reviews
(2000) - et al.
Methanogenic population structure in a variety of anaerobic bioreactors
FEMS Microbiology Letters
(2003) - et al.
Nitrification-denitrification dynamics and community structure of ammonia oxidizing bacteria in a high yield irrigated Philippine rice field
FEMS Microbiology Ecology
(2004) - et al.
Identification of novel Crenarchaeota and Euryarchaeota clusters associated with different depth layers of a forest soil
FEMS Microbiology Ecology
(2002) - et al.
Effects of freeze-thaw of stress during soil storage on microbial communities and methidation degradation
Soil Biology Biochemistry
(2003) - et al.
Archaeal diversity and community structure in a Swedish barley field: specificity of the Ek510r/(EURY498) 16S rDNA primer
Journal of Microbiology Methods
(2007) The distribution and diversity of Euryarchaeota in termite guts
Advances in Applied Microbiology
(2007)