Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties
TL;DR: History of land-use was a stronger determinant of the composition of microbial communities than vegetation and soil properties, and microbial communities in disturbed soils apparently return to their native state with time.
Abstract: The response of soil microbial communities following changes in land-use is governed by multiple factors. The objectives of this study were to investigate (i) whether soil microbial communities track the changes in aboveground vegetation during succession; and (ii) whether microbial communities return to their native state over time. Two successional gradients with different vegetation were studied at the W. K. Kellogg Biological Station, Michigan. The first gradient comprised a conventionally tilled cropland (CT), mid-succession forest (SF) abandoned from cultivation prior to 1951, and native deciduous forest (DF). The second gradient comprised the CT cropland, early-succession grassland (ES) restored in 1989, and long-term mowed grassland (MG). With succession, the total microbial PLFAs and soil microbial biomass C consistently increased in both gradients. While bacterial rRNA gene diversity remained unchanged, the abundance and composition of many bacterial phyla changed significantly. Moreover, microbial communities in the relatively pristine DF and MG soils were very similar despite major differences in soil properties and vegetation. After >50 years of succession, and despite different vegetation, microbial communities in SF were more similar to those in mature DF than in CT. In contrast, even after 17 years of succession, microbial communities in ES were more similar to CT than endpoint MG despite very different vegetation between CT and ES. This result suggested a lasting impact of cultivation history on the soil microbial community. With conversion of deciduous to conifer forest (CF), there was a significant change in multiple soil properties that correlated with changes in microbial biomass, rRNA gene diversity and community composition. In conclusion, history of land-use was a stronger determinant of the composition of microbial communities than vegetation and soil properties. Further, microbial communities in disturbed soils apparently return to their native state with time.
Citations
More filters
TL;DR: It is found that the agricultural and early successional land uses harbored unique soil bacterial communities that exhibited distinct temporal patterns that were likely a product of complex interactions between the soil environment and the more diverse plant community.
Abstract: Although numerous studies have investigated changes in soil microbial communities across space, questions about the temporal variability in these communities and how this variability compares across soils have received far less attention. We collected soils on a monthly basis (May to November) from replicated plots representing three land-use types (conventional and reduced-input row crop agricultural plots and early successional grasslands) maintained at a research site in Michigan, USA. Using barcoded pyrosequencing of the 16S rRNA gene, we found that the agricultural and early successional land uses harbored unique soil bacterial communities that exhibited distinct temporal patterns. α-Diversity, the numbers of taxa or lineages, was significantly influenced by the sampling month with the temporal variability in α-diversity exceeding the variability between land-use types. In contrast, differences in community composition across land-use types were reasonably constant across the 7-month period, suggesting that the time of sampling is less important when assessing β-diversity patterns. Communities in the agricultural soils were most variable over time and the changes were significantly correlated with soil moisture and temperature. Temporal shifts in bacterial community composition within the successional grassland plots were less predictable and are likely a product of complex interactions between the soil environment and the more diverse plant community. Temporal variability needs to be carefully assessed when comparing microbial diversity across soil types and the temporal patterns in microbial community structure can not necessarily be generalized across land uses, even if those soils are exposed to the same climatic conditions.
402 citations
Cites background or result from "Land-use history has a stronger imp..."
...The differences between the cultivated and early successional grassland plots (Figure 3a) mirror those reported previously where agricultural and non-agricultural soils (even those located in close proximity) often harbor distinct communities (Buckley and Schmidt, 2001a; Bissett et al., 2011; Jangid et al., 2011)....
[...]
...…between the cultivated and early successional grassland plots (Figure 3a) mirror those reported previously where agricultural and non-agricultural soils (even those located in close proximity) often harbor distinct communities (Buckley and Schmidt, 2001a; Bissett et al., 2011; Jangid et al., 2011)....
[...]
TL;DR: The trade-offs between the use of cellulosic biofuels and climate mitigation, biodiversity, reactive nitrogen loss, and water use are reviewed to direct more effective policies for their production.
Abstract: Cellulosic crops are projected to provide a large fraction of transportation energy needs by mid-century. However, the anticipated land requirements are substantial, which creates a potential for environmental harm if trade-offs are not sufficiently well understood to create appropriately prescriptive policy. Recent empirical findings show that cellulosic bioenergy concerns related to climate mitigation, biodiversity, reactive nitrogen loss, and crop water use can be addressed with appropriate crop, placement, and management choices. In particular, growing native perennial species on marginal lands not currently farmed provides substantial potential for climate mitigation and other benefits.
312 citations
TL;DR: This review explores key drivers for microbial life in soils under different climates and land-use practices at scales ranging from soil pores to landscapes and delineates special features of soil as a microbial habitat and the consequences for microbial communities.
Abstract: Soil, the living terrestrial skin of the Earth, plays a central role in supporting life and is home to an unimaginable diversity of microorganisms. This review explores key drivers for microbial life in soils under different climates and land-use practices at scales ranging from soil pores to landscapes. We delineate special features of soil as a microbial habitat (focusing on bacteria) and the consequences for microbial communities. This review covers recent modeling advances that link soil physical processes with microbial life (termed biophysical processes). Readers are introduced to concepts governing water organization in soil pores and associated transport properties and microbial dispersion ranges often determined by the spatial organization of a highly dynamic soil aqueous phase. The narrow hydrological windows of wetting and aqueous phase connectedness are crucial for resource distribution and longer range transport of microorganisms. Feedbacks between microbial activity and their immediate environment are responsible for emergence and stabilization of soil structure-the scaffolding for soil ecological functioning. We synthesize insights from historical and contemporary studies to provide an outlook for the challenges and opportunities for developing a quantitative ecological framework to delineate and predict the microbial component of soil functioning.
283 citations
TL;DR: The evidence supports the conclusion that most bacterial and archaeal taxa remain uncultured, as sequence similarity cannot be used to infer “culturability" because one cannot infer physiology from 16S rRNA gene sequences.
Abstract: A recent paper by Martiny argues that “high proportions” of bacteria in diverse Earth environments have been cultured. Here we reanalyze a portion of the data in that paper, and argue that the conclusion is based on several technical errors, most notably a calculation of sequence similarity that does not account for sequence gaps, and the reliance on 16S rRNA gene amplicons that are known to be biased towards cultured organisms. We further argue that the paper is also based on a conceptual error: namely, that sequence similarity cannot be used to infer “culturability” because one cannot infer physiology from 16S rRNA gene sequences. Combined with other recent, more reliable studies, the evidence supports the conclusion that most bacterial and archaeal taxa remain uncultured.
229 citations
TL;DR: It was found that zero tillage most affected the bacterial communities, while crop residue management affected the microbial communities more than when conventional tillage was applied, indicating that even though phylotypes changed, the number and diversity of theacterial communities were similar.
Abstract: In this study, the effect of limited tillage versus traditional tillage, residue retention versus removal and crop rotation (maize–wheat) versus monoculture (maize) on the bacterial community structure in soils was investigated by means of 454 pyrosequencing of the 16S rRNA gene. Using taxonomic and phylogenetic information it was found that zero tillage most affected the bacterial communities. The relative abundance of Actinobacteria, Betapreoteobacteria and Gammaproteobacteria was affected by tillage and correlated to the total organic carbon (TOC) and clay content in soil. Residue management had a significant effect on the bacterial community structure when phylogenetic membership and the total enumeration of bacteria were considered. Residue management affected the relative abundance of Bacteroidetes, Betaproteobacteria, Cyanobacteria and Gemmatimonadetes. When no tillage was applied, crop residue management affected the microbial communities more than when conventional tillage was applied. Wheat–maize rotation or crop monoculture did not affect the bacterial community structure. No significant differences in richness, diversity and total abundance of bacteria was found between the treatments. This indicated that even though phylotypes changed, the number and diversity of the bacterial communities were similar.
223 citations
Cites background from "Land-use history has a stronger imp..."
...For instance, some authors reported a significant effect on microbial biomass or bacterial composition as a consequence of the tillage practice (Kihara et al., 2012; Lupwayi et al., 2012), while others reported no effect (Jangid et al., 2011; Jiang et al., 2011)....
[...]
..., 2012), while others reported no changes in diversity and richness (Hartmann and Widmer, 2006; Jangid et al., 2011; Jiang et al., 2011)....
[...]
...It has often been debated if soil physicochemical factors or the land-use practices shape the bacterial communities in terrestrial environments (Jangid et al., 2011; Kuramae et al., 2012)....
[...]
...These groups are often dominant in agricultural and other soil ecosystems (Lauber et al., 2008; Faoro et al., 2010; Yin et al., 2010; Jangid et al., 2011; Nemergut et al., 2011; Bernard et al., 2012)....
[...]
...Several studies have found that fungal and bacterial diversity is higher in soils under zero tillage than tilled soils (Lupwayi et al., 2004, 2012; Kihara et al., 2012), while others reported no changes in diversity and richness (Hartmann and Widmer, 2006; Jangid et al., 2011; Jiang et al., 2011)....
[...]
References
More filters
TL;DR: A 16S rRNA gene database (http://greengenes.lbl.gov) was used to provide chimera screening, standard alignment, and taxonomic classification using multiple published taxonomies as mentioned in this paper.
Abstract: A 16S rRNA gene database (http://greengenes.lbl.gov) addresses limitations of public repositories by providing chimera screening, standard alignment, and taxonomic classification using multiple published taxonomies. It was found that there is incongruent taxonomic nomenclature among curators even at the phylum level. Putative chimeras were identified in 3% of environmental sequences and in 0.2% of records derived from isolates. Environmental sequences were classified into 100 phylum-level lineages in the Archaea and Bacteria.
9,593 citations
TL;DR: Bacterial diversity was highest in neutral soils and lower in acidic soils, with soils from the Peruvian Amazon the most acidic and least diverse in this study.
Abstract: For centuries, biologists have studied patterns of plant and animal diversity at continental scales. Until recently, similar studies were impossible for microorganisms, arguably the most diverse and abundant group of organisms on Earth. Here, we present a continental-scale description of soil bacterial communities and the environmental factors influencing their biodiversity. We collected 98 soil samples from across North and South America and used a ribosomal DNA-fingerprinting method to compare bacterial community composition and diversity quantitatively across sites. Bacterial diversity was unrelated to site temperature, latitude, and other variables that typically predict plant and animal diversity, and community composition was largely independent of geographic distance. The diversity and richness of soil bacterial communities differed by ecosystem type, and these differences could largely be explained by soil pH (r(2) = 0.70 and r(2) = 0.58, respectively; P < 0.0001 in both cases). Bacterial diversity was highest in neutral soils and lower in acidic soils, with soils from the Peruvian Amazon the most acidic and least diverse in our study. Our results suggest that microbial biogeography is controlled primarily by edaphic variables and differs fundamentally from the biogeography of "macro" organisms.
4,376 citations
"Land-use history has a stronger imp..." refers background in this paper
..., 2010), salinity (Lozupone and Knight, 2007; Rajaniemi and Allison, 2009) and pH (Fierer and Jackson, 2006), have a significant impact on the structure of soil microbial communities....
[...]
...Soil properties, such as soil type (Wu et al., 2008; Bach et al., 2010; Jangid et al., 2010), salinity (Lozupone and Knight, 2007; Rajaniemi and Allison, 2009) and pH (Fierer and Jackson, 2006), have a significant impact on the structure of soil microbial communities....
[...]
TL;DR: A computer program, DOTUR, is developed, which assigns sequences to OTUs by using either the furthest, average, or nearest neighbor algorithm for each distance level, which addresses the challenge of assigning sequences to operational taxonomic units (OTUs) based on the genetic distances between sequences.
Abstract: Although copious qualitative information describes the members of the diverse microbial communities on Earth, statistical approaches for quantifying and comparing the numbers and compositions of lineages in communities are lacking. We present a method that addresses the challenge of assigning sequences to operational taxonomic units (OTUs) based on the genetic distances between sequences. We developed a computer program, DOTUR, which assigns sequences to OTUs by using either the furthest, average, or nearest neighbor algorithm for each distance level. DOTUR uses the frequency at which each OTU is observed to construct rarefaction and collector's curves for various measures of richness and diversity. We analyzed 16S rRNA gene libraries derived from Scottish and Amazonian soils and the Sargasso Sea with DOTUR, which assigned sequences to OTUs rapidly and reliably based on the genetic distances between sequences and identified previous inconsistencies and errors in assigning sequences to OTUs. An analysis of the two 16S rRNA gene libraries from soil demonstrated that they do not contain enough sequences to support a claim that they contain different numbers of bacterial lineages with statistical confidence (P > 0.05), nor do they contain enough sequences to provide a robust estimate of species richness when an OTU is defined as containing sequences that are no more than 3% different from each other. In contrast, the richness of OTUs at the 3% level in the Sargasso Sea collection began to plateau after the sampling of 690 sequences. We anticipate that an equivalent extent of sampling for soil would require sampling more than 10,000 sequences, almost 100 times the size of typical sequence collections obtained from soil.
2,314 citations
"Land-use history has a stronger imp..." refers methods in this paper
...03 using the average neighbor algorithm in DOTUR (Schloss and Handelsman, 2005)....
[...]
...Shannon diversity index (H), Chao1 estimate, and reciprocal of Simpson’s index (1/D) were calculated based on the number of operational taxonomic units (OTUs) at an evolutionary distance (D) of 0.03 using the average neighbor algorithm in DOTUR (Schloss and Handelsman, 2005)....
[...]
TL;DR: The most comprehensive analysis of the environmental distribution of bacteria to date, based on 21,752 16S rRNA sequences compiled from 111 studies of diverse physical environments, is reported in this article.
Abstract: Microbes are difficult to culture. Consequently, the primary source of information about a fundamental evolutionary topic, life's diversity, is the environmental distribution of gene sequences. We report the most comprehensive analysis of the environmental distribution of bacteria to date, based on 21,752 16S rRNA sequences compiled from 111 studies of diverse physical environments. We clustered the samples based on similarities in the phylogenetic lineages that they contain and found that, surprisingly, the major environmental determinant of microbial community composition is salinity rather than extremes of temperature, pH, or other physical and chemical factors represented in our samples. We find that sediments are more phylogenetically diverse than any other environment type. Surprisingly, soil, which has high species-level diversity, has below-average phylogenetic diversity. This work provides a framework for understanding the impact of environmental factors on bacterial evolution and for the direction of future sequencing efforts to discover new lineages.
1,440 citations
TL;DR: Soil pH was the best predictor of bacterial community composition across this landscape while fungal community composition was most closely associated with changes in soil nutrient status, suggesting specific changes in edaphic properties, not necessarily land-use type itself, may best predict shifts in microbialcommunity composition across a given landscape.
Abstract: Land-use change can have significant impacts on soil conditions and microbial communities are likely to respond to these changes. However, such responses are poorly characterized as few studies have examined how specific changes in edaphic characteristics do, or do not, influence the composition of soil bacterial and fungal communities across land-use types. Soil samples were collected from four replicated ( n = 3) land-use types (hardwood and pine forests, cultivated and livestock pasture lands) in the southeastern US to assess the effects of land-use change on microbial community structure and distribution. We used quantitative PCR to estimate bacterial–fungal ratios and clone libraries targeting small-subunit rRNA genes to independently characterize the bacterial and fungal communities. Although some soil properties (soil texture and nutrient status) did significantly differ across land-use types, other edaphic factors (e.g., pH) did not vary consistently with land-use. Bacterial–fungal ratios were not significantly different across the land-uses and distinct land-use types did not necessarily harbor distinct soil fungal or bacterial communities. Rather, the composition of bacterial and fungal communities was most strongly correlated with specific soil properties. Soil pH was the best predictor of bacterial community composition across this landscape while fungal community composition was most closely associated with changes in soil nutrient status. Together these results suggest that specific changes in edaphic properties, not necessarily land-use type itself, may best predict shifts in microbial community composition across a given landscape. In addition, our results demonstrate the utility of using sequence-based approaches to concurrently analyze bacterial and fungal communities as such analyses provide detailed phylogenetic information on individual communities and permit the robust assessment of the biogeographical patterns exhibited by soil microbial communities.
1,420 citations
"Land-use history has a stronger imp..." refers background in this paper
...While texture and other physicochemical properties of soil correlated with community structure in this gradient and other soils (Lauber et al., 2008; Tarlera et al., 2008), it was not observed for the...
[...]
...While texture and other physicochemical properties of soil correlated with community structure in this gradient and other soils (Lauber et al., 2008; Tarlera et al., 2008), it was not observed for the MI.a Table 6 Abundance of specific OTUs in the 16S rRNA gene libraries.a GASP clone…...
[...]
...Likewise, Lauber et al. (2008) observed similarities in microbial communities between >40-year-old pastures that had been grazed and >75- year-old oak-hickory forests in South Carolina....
[...]