Shifting prokaryotic communities along a soil formation chronosequence and across soil horizons in a South Taiga ecosystem
Graphical abstract
Introduction
The study of the peculiarities of pedogenic processes and soil evolution are central issues in soil science. Pedogenesis is a complex process, involving the interaction of abiotic (climate, parent materials) (Cerli et al., 2008; Huggett, 1998) and biogenic factors, and in this context, soil formation and development may be affected by the structure, abundance, and activity of the soil microbial community. The vertical and spatial patterns of the soil profile, therefore, illustrate not only the specific combination of environmental conditions (resulting in differences in the physicochemical parameters of genetic horizons), but also reflect the processes of specific adaptive and evolutionary scenarios of soil microbial complexes.
The use of a metagenomic approach allows the analysis of the entire microbial diversity, including uncultured groups of microorganisms, and therefore, provides new opportunities for studying the process of soil formation. However, metagenomic soil studies are complicated by the spatial heterogeneity of soil ecosystems, associated, in particular, with the formation of genetic horizons, and often sharply differ in several physical and chemical parameters. These differences in environmental conditions within soil horizons, which increase during the evolution of the latter, are expected to affect the structure of micro-organisms, which quickly adapt to changes in environmental conditions. Therefore, soil and its microbiome should be considered a developing system, and the composition and structure of the microbial complex can act as an ecological indicator, marking the main trends in the evolution and ecogenesis of the soil profile.
Changes in the physicochemical properties of soil with increasing depth cause substantial shifts in the structure of the microbial community. The differences between microbial community structures in individual horizons in the profile may be more noticeable than changes in the microbiome pattern in soil surface horizons of a wide range of biomes (Eilers et al., 2012; Chernov et al., 2017). This finding explains the increasing attention researchers are directing to the belowground layers of the soil in recent times (Eilers et al., 2012; Semenov et al., 2018). According to some estimations, subsurface horizons contain up to 35–50% of the total microbial biomass (Fierer et al., 2003; Schütz et al., 2010).
One way to investigate the subsurface microbiome is the separation and sampling of soil by depth (Eilers et al., 2012; Jiao et al., 2018). The advantage of this method is the relative simplicity and formalization of soil sampling. However, evaluation of the evolutionary trends of pedogenesis is lacking. Another strategy is the isolation of individual genetic soil horizons (Will et al., 2010; Chernov et al., 2017; Semenov et al., 2018). To date, only a few studies have applied this approach to distinguish the microbial patterns associated specifically with A (organic) and B (mineral) horizons (Will et al., 2010; Chernov et al., 2017; Semenov et al., 2018). The isolation of morphologically, as well as physically, chemically, and biologically different horizons, has been a central issue for soil science in Russia for centuries. The great variety of Russian soils, together with the vast undisturbed areas of Russian federal reserves and national parks, provide a unique opportunity to investigate different stages of soil formation in the natural chronosequences of different types of soils. The investigation of the soil profile in a chronosequence allows the tracing of the evolution of soil horizon over time, which is very promising for evaluating the evolutionary trends in the soil microbiome during pedogenesis and ecosystem development.
Many studies have been devoted to the study of soil chronosequences. Today, the morphological descriptions of soil chronocatena (Abakumov et al., 2010; Cerli et al., 2008, 2006) and estimations of the biomass, as well as the metabolic activity and diversity of cultivated microorganisms in soils, already exist (Frouz and Novakowa, 2005; Šourková et al., 2005). The main advantage of these data for metagenomic studies is precise dating as it reveals the specific microbial groups and diversity patterns, possibly marking the ecogenetic stages of soil formation.
The study of differently-aged coastal bars, presented by sandy textured parent materials, has long been regarded as important in evolutionary soil science. Historically, soils of different ages formed on the sands have been the main object of the study of soil formation processes in the taiga zone; the chronosequence of soil restoration and ecosystems recovered by vegetation are often found here (Alexandrovsky et al., 2012). The soil chronosequence on the coastal bars of Lake Ladoga is the most representative model of soil formation on sandy rocks (Aleksandrovsky et al., 2009) versus the other models available (e.g., chronocatens in quarries, dunes, and soils under burrows).
In this context, our study aimed to analyze the structure and distribution of microbiomes in profiles of soil chronosequences under conditions of a long-term soil-forming process occurring on the surface of differently-aged coastal transgression bars of the Nizhnesvirsky Reserve. Since the earliest point of dated soil formation was 70 years and the latest was 1,590 years (Abakumov et al., 2019), we had an opportunity to fully characterize the process of soil formation from the embryonic stage to the climax podzol. The main objectives of this work were: 1) the analysis of the diversity of prokaryotic complexes in the podzol soil chronosequences; 2) ascertaining the specific features of the taxonomic composition associated both with the genetic horizon appearance and its evolution; and 3) the determination of key physicochemical soil parameters influencing the structure and diversity of prokaryotic communities.
Section snippets
A brief description of the environmental conditions and soil-forming processes in the territory of the Nizhnesvirsky Nature Reserve
The Nizhnesvirsky Nature Reserve was established in 1980 on the site of a local specially protected area in south-eastern Priladozhie, in the territory of the Leningrad region of North-West Russia. The Nizhnesvirsky Nature Reserve is located in the Ladoga lowlands and is bounded on the south and east by the Svir River, and in the west by Svir Bay on Lake Ladoga, part of which is included in the reserve. The northern border is both the border of the Leningrad region and Karelia. The area of the
Analysis of qPCR data
Quantitative analysis revealed the accumulation of bacteria and archaea in the topsoil (organic horizons), with a relative decrease in prokaryotic ribosomal operon abundances with soil depth (Fig. 1). A steep decrease, especially in young soils, in bacterial abundance in the mineral horizons was noted. The content of the archaeal operons showed some profile differentiation by the eluvial-illuvial pattern, with significant accumulation in the deep horizons of mature soils (2BF1 and 2 G horizons).
Discussion
The soils that formed on the surfaces of the transgressive bars of the Nizhnesvirsky Nature Reserve represent a living example of soil ergodicity (wherein a soil body has spatial analogs corresponding to the chronological stages of its development) (Abakumov, 2011). Soil chronosequences (water terraces, chronosequences of soils on dunes and under barrows, uneven-aged soils in quarries) are widely studied in modern evolutionary genetic soil science (Huggett, 1998; Frouz, 2014; Kurbanova et al.,
Conclusions
The soils formed on the surface of the transgressive bars of the Nizhnesvirsky Reserve represent a vivid illustration of the implementation of the podzol-formation process in the southern taiga zone, which allows their utilization as a model to retrospectively assess the development of podzolic soils and the spatial and temporal dynamics of soil microorganism complexes. Considering the high genetic and metabolic potential of the soil microbiome, one can logically assume that the development of
Funding
This work was supported by the grant no. 17-16-01030 of the Russian Science Foundation.
Declaration of Competing Interest
Authors declare that there is no conflict of interest.
Acknowledgements
Authors would like to thank Nadezda Vasilieva, the Head of the Interdisciplinary Laboratory for Mathematical Modeling of Soil Systems, V.V. Dokuchaev Soil Science Institute, for advising and help in the statistical processing of some of the results obtained. Also, we thank the anonymous referees for their useful suggestions.
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