Global biogeographic distribution of Bathyarchaeota in paddy soils

Abstract

Bathyarchaeota, known as key participants of global elements cycling, is highly abundant and diverse in the sedimentary environments. Bathyarchaeota has been the research spotlight on sedimentary microbiology; however, its distribution in arable soils is far from understanding. Paddy soil is a habitat similar to freshwater sediments, while the distribution and composition of Bathyarchaeota in paddy soils have largely been overlooked. In this study, we collected 342 in situ paddy soil sequencing data worldwide to illuminate the distribution patterns of Bathyarchaeota and explore their potential ecological functions in paddy soils. The results showed that Bathyarchaeota is the dominant archaeal lineage, and Bathy-6 is the most predominant subgroup in paddy soils. Based on random forest analysis and construction of a multivariate regression tree, the mean annual precipitation and mean annual temperature are identified as the factors significantly influencing the abundance and composition of Bathyarchaeota in paddy soils. Bathy-6 was abundant in temperate environments, while other subgroups were more abundant in sites with higher rainfall. There are highly frequent associations between Bathyarchaeota and methanogens and ammonia-oxidizing archaea. The interactions between Bathyarchaeota and microorganisms involved in carbon and nitrogen metabolism imply a potential syntrophy between these microorganisms, suggesting that members of Bathyarchaeota could be important participants of geochemical cycle in paddy soils. These results shed light on the ecological lifestyle of Bathyarchaeota in paddy soils, and provide some baseline for further understanding Bathyarchaeota in arable soils. IMPORTANCE Bathyarchaeota, the dominant archaeal lineage in sedimentary environments, has been the spotlight of microbial research due to its vital role in carbon cycling. Although Bathyarchaeota has been also detected in paddy soils worldwide, its distribution in this environment has not yet been investigated. In this study, we conducted a global scale meta-analysis and found that Bathyarchaeota is also the dominant archaeal lineage in paddy soils with significant regional abundance differences. Bathy-6 is the most predominant subgroup in paddy soils, which differs from sediments. Furthermore, Bathyarchaeota are highly associated with methanogens and ammonia-oxidizing archaea, suggesting that they may be involved in the carbon and nitrogen cycle in paddy soil. These interactions provide insight into the ecological functions of Bathyarchaeota in paddy soils, which will be the foundation of future studies regarding the geochemical cycle in arable soils and global climate change.

Biogeography and niche differentiation of Bathyarchaeia in paddy soils across eastern China

“…Concerning the community structure of Bathyarchaeia in paddy soils, the Bathy-6 subgroup exclusively predominates across all surveyed sites, accompanied by a smaller representation of ASVs associated with Bathy-11 , Bathy-15 , Bathy-5bb , andBathy-17 . In comparison with our recent meta-analysis (Xue et al 2023), the subgroup diversity of Bathyarchaeia in paddy soils within eastern China (comprising 5 subgroups) appeared lower than the global scale (comprising 7 subgroups), as Bathy-18 andBathy-5b were not detected in our study. This discrepancy might be elucidated by the greater diversity observed in paddy soils worldwide.…”

“…4). This observation harmonizes with our recent global meta-analysis (Xue et al 2023), underscoring the influence of temperature on Bathyarchaeiasubgroups in soils, as similarly documented by previous study (Xiang et al 2017), who explored the impact of temperature onBathyarchaeia subgroups in soils via multivariate regression tree analysis (Xiang et al 2017). The discovery of Bathyarchaeia in hot springs further accentuates its remarkable adaptability to high-temperature environments (Barns et al 1996).…”

“…Bathyarchaeia also frequently co-occurred with members ofNitrososphaeria (Fig. 5d), which is consistent with the results of the global meta-analysis (Xue et al 2023). Nitrososphaeria is a group of ammoniaoxidizing archaea highly abundant in rice rhizosphere soil with fertilization (Tang et al 2019).…”

“…A recent global meta-analysis reported that Bathyarchaeia is globally distributed in paddy soils with high abundance, and the predominant subgroup is Bathy-6 (Xue et al 2023). The meta-analysis showed that the mean annual precipitation and the mean annual temperature could be associated with the relative abundance of Bathyarchaeia and Bathyarchaeial community structure, respectively (Xue et al 2023). However, this meta-analysis had some limitations, such as the limited availability of soil physicochemical parameters data and distribution.…”