Bacterial Communities in a Buried Ancient Paddy Soil from the Neolithic Age

doi:10.1016/S1002-0160(10)60028-8

Pedosphere

Volume 20, Issue 3, June 2010, Pages 389-398

https://doi.org/10.1016/S1002-0160(10)60028-8 Get rights and content

Abstract

An ancient irrigated paddy soil from the Neolithic age was excavated at Chuodunshan Site in the Yangtze River Delta, close to Suzhou, China. The soil organic matter (SOM) content in the prehistoric rice soil is comparable to the average SOM content of present rice soils in this region, but it is about 5 times higher than that in the parent materials. As possible biomarkers to indicate the presence of the prehistoric paddy soil, the bacterial communities were investigated using the techniques of aerobic and anaerobic oligotrophic bacteria enumeration, Biolog analysis, and polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE). The results showed that in the buried soil layers, the prehistoric paddy soil had the largest number of aerobic and anaerobic oligotrophic bacteria, up to 6.12 and 5.86 log cfu g⁻¹ dry soil, respectively. The prehistoric paddy soil displayed better carbon utilization potential and higher functional diversity compared to the parent materials and a prehistoric loess layer. The Shannon index and richness based on DGGE profiles of bacterial 16S rRNA genes were higher in prehistoric paddy soil than those in the prehistoric loess soil. It might be concluded that the prehistoric irrigated rice cultivation accumulated the SOM in plowed soil layer, and thus increased soil bacterial populations, metabolic activity, functional diversity and genetic diversity. Bacterial communities might be considered as the sensitive indicators of the presence of the prehistoric paddy soil in China's Yangtze River Delta.

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In this study, the highest abundance of archaeol and GDGT-0 were observed in deeper parts of the profiles (P01B and P04C), indicating that those lipids are likely fossil records rather than the contemporary production of extant archaea. On the other hand, studies have revealed that current methane formation from microbial activities are quite low in ancient buried paddy soils (Shen et al., 2006, 2010), which implies that epigenetic archaea in the ancient paddy soils may be inactive and have negligible influence on the archaeal lipid pool. Furthermore, these variations of archaeal lipid abundances are concordant with the PLFA results and bacterial 16S rRNA pyrosequencing data in these two profiles, in which samples of the current (long-term) cultivated paddy soils have a higher PLFA concentration and bacterial diversity than ancient buried paddy soils (Zhu et al., 2016a), indicating that extant bacteria, as well as archaea, may not be active in the buried ancient paddy soils.
Paddy soil is the consequence of human activity, which has exerted significant anthropogenic impacts on the global carbon cycle in recent earth history, particularly through the production of microbial methane from paddy soils. However, the anthropogenic impact of rice fields on the distribution of methanogenic archaea and methane emission during human history is poorly documented. Isoprenoid glycerol dialkyl glycerol tetraethers (iGDGTs) are unique biomarkers for archaea, which can be used to examine changes in climate and environment during human evolution. This study aimed to reconstruct archaeal communities and evaluate how they might have been impacted by human activities during the development of two paddy soil profiles that recorded a cultivation history of over 6300 years in Zhejiang Province, southeastern China. Variations in archaeol, GDGT-0 and crenarchaeol strongly suggest that archaeal ether lipids deeply buried in the ancient paddy soil profiles are mainly fossil records rather than contemporary signals. Cluster analysis based on GDGT compositions revealed two major groups of GDGTs corresponding to different soil types, reflecting the shift of archaeal communities from Thaumarchaeota to methanogens. The archaeal ether lipid-based proxies (MI, archaeol/crenarchaeol and GDGT-0/crenarchaeol) related to methane-producing archaea varied remarkably in different soil types associated with the anthropogenic management. These proxies had significantly higher values in the buried paddy soils than currently cultivated paddy soils, implying that the earlier anthropogenic flooding may have resulted in considerable methane emission from paddy soils in southeastern China.
The influence of soil properties on the size and structure of bacterial and fungal communities along a paddy soil chronosequence
2016, European Journal of Soil Biology
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However, micro-organisms (e.g., bacteria, fungi, and protozoa) may not be sensitive to short-term consequences of conversion (disturbance, loss of habitat) but predominantly be affected by long-term changes in soil properties (probably loss of organic matter) [40]. Ancient paddy soil tend to accumulate more soil organic matter in the plowed soil layer with increased soil bacterial populations, higher metabolic activity, and greater functional diversity and genetic diversity than present day paddy soils [47]. The development of paddy soils with time has also been reflected in the increased activity of one particular subgroup of methanotrophs [22].
In agroecosystems, soil bacterial and fungal communities are crucial for soil and plant health because of their diverse metabolic functions. However, little is known about the effect of long term paddy management on microbial communities. This study was conducted to assess the responses of the soil bacterial and fungal communities to cultivation history along a paddy soil chronosequence by using phospholipid fatty acid (PLFA) profiling and Illumina HiSeq sequencing. Soil samples were collected from the paddy fields (50, 100, 300, 1000, and 2000 years of paddy use; P50-P2000-), the adjacent arable chronosequence (50, 100 and 300 years of land use; NP50-NP300) and mudflat (estuarine sediment, representing the parent material for paddy and arable soil reclamation). The results showed that soil microbial biomass PLFAs increased significantly with increasing soil organic C which accumulated more under paddy than arable management. Bacterial taxonomic groups assigned to Proteobacteria and Acidobacteria changed relatively in the transition from tidal wetland to agricultural land. The relative abundances of dominant bacterial phyla in paddy soil orderly changes with cultivation time. The dominant fungal phyla in all samples were Ascomycota, Chytridiomycota, Basidiomycota, Glomeromycota and Zygomycota, representing 18.50%, 18.46%, 10.02%, 7.34%, and 7.19%, respectively. The succession of fungal community structure was mainly associated with changes in Ascomycota. Correlation analysis showed that higher soil total carbon and nitrogen related to long-term cultivation were associated with lower Proteobacteria and Ascomycota, but higher Verrucomicrobia. Furthermore, different land use type differed significantly in their fungal composition, but likely had similar effects on the succession of bacterial composition, mainly the Proteobacteria and Acidobacteria. Our results indicate that orderly succession of soil bacterial and fungal communities occurred along the long-term development of paddy soil, which in turn was associated with changes in soil physicochemical properties over time.
A buried Neolithic paddy soil reveals loss of microbial functional diversity after modern rice cultivation
2016, Science Bulletin
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To further verify if the buried soil was paddy soil, phytolith from both buried and currently cultivated paddy soils were extracted and examined. The phytolith concentration of soil samples were all beyond 5000 grains g−1 (Table S3), providing evidence of rice cultivation in the sampling field [40], which is also supported by earlier archeological data on this Neolithic paddy soil [41]. The natural 15N abundance of buried ancient soils was markedly higher than that of the currently cultivated soils (Table S3), indicating the use of chemical N fertilizers in modern rice production, as chemical fertilizers have considerably lower 15N abundance [42].
It has been documented that human activities are causing the rapid loss of taxonomic, phylogenetic, genetic and functional diversity in soils. However, it remains unclear how modern intensive rice cultivation impacts the soil microbiome and its functionality. Here we examined the microbial composition and function differences between a buried Neolithic paddy soil and an adjacent, currently-cultivated paddy soil using high throughput metagenomics technologies. Our results showed that the currently cultivated soil contained about 10-fold more microbial biomass than the buried one. Analyses based on both 16S rRNA genes and functional gene array showed that the currently cultivated soil had significantly higher phylogenetic diversity, but less functional diversity than the buried Neolithic one. The community structures were significantly different between modern and ancient soils, with functional structure shifting towards accelerated organic carbon (C) degradation and nitrogen (N) transformation in the modern soils. This study implies that, modern intensive rice cultivation has substantially altered soil microbial functional structure, leading to functional homogenization and the promotion of soil ecological functions related to the acceleration of nutrient cycling which is necessary for high crop yields.
Comparative Analysis of the Structure of Buried and Surface Soils by Analysis of Microbial DNA
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Microbial dna analyses of soils buried under earthworks
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: Supported by the National Natural Science Foundation of China (No. 40335047) and the Sino-German Center for Research Promotion in Beijing (No. GZ 518).

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Bacterial Communities in a Buried Ancient Paddy Soil from the Neolithic Age

Abstract

FEMS Microbiol. Ecol.

Mutat. Res. Genomics.

Soil Biol. Biochem.

J. Microbiol. Meth.

Geoderma.

Agr. Sci. China.

Anal. Chim. Acta.

FEMS Microbiol. Ecol.

Soil Biol. Biochem.

Soil Biol. Biochem.

Ancient paddy soils from the Neolithic age in China's Yangtze River Delta

Naturwissenschaften.

The origin, evolotion, cultivation, dissemination and diversification of Asian and African rices

Euphytica.

Principles and Practices of Rice Production

Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization

Appl. Environ. Microb.

Prehistorically modified soils of central Amazonia: a model for sustainable agriculture in the twenty-first century

Philos. T. Roy. Soc. B.

Formation and classification of anthrosols: China's perspectives

The Sustainability of Rice Farming