Elsevier

Pedobiologia

Volumes 81–82, September 2020, 150650
Pedobiologia

Shifting prokaryotic communities along a soil formation chronosequence and across soil horizons in a South Taiga ecosystem

https://doi.org/10.1016/j.pedobi.2020.150650Get rights and content

Highlights

  • The structure of the soil microbiome is horizon- and age- specific within the soil chonosequence.

  • The organic and stagnic horizons were most variable in terms of microbiome structure.

  • The difference of prokaryotes’ structure of genetic horizons were revealed both at high and low taxonomic level.

  • The dissimilarity between organic and mineral horizons is increasing with soil age.

Abstract

The study of chronosequences allows the analysis of the temporal and spatial dynamics of ecogenesis, soil microbiome and soil development. Here, we investigated the taxonomic diversity of bacterial and archaeal communities along a chronosequence of soils that formed on four Lake Ladoga coastal bars in the Nizhnesvirsky Nature Reserve (Leningrad region, north-west Russian Federation). We analyzed two factors: the age of sampled solum (ranging from 70 to 1,590 years) and the soil horizons that differ in terms of morphology and genesis.

We observed a relationship between podzolisation, typical major soil-forming processes of the southern taiga zone, and the taxonomic structure of prokaryotic communities. The most pronounced differences between microbial communities were associated with the vertical heterogeneity of soil profile. Phyla associated with copiotrophic habits (Proteobacteria, Actinobacteria and Bacteroidetes) were more frequent in topsoil. Podzolic eluvial (E) horizons had higher frequencies of the genus Mycobacterium (Actinobacteria). In deeper horizons, we observed lower frequencies of copiotrophic phyla and increased frequencies of phyla associated with oligotrophic habits (Nitrospirae, Gemmatomonadetes, Planctomycetes, Chloroflexi, etc.), as well as archaeal lineages. The lowest (gleyic, G) horizons had high frequencies of anaerobic and methane-producing bacteria.

Therefore, the relationship between microbial community structure and the continuous development of the soil profile was revealed. Shifting physico-chemical were identified as key factors associated with variation in prokaryotic communities. The older coastal bar demonstrated the clearer signs of podzol formation, increased thickness of the E horizon, and increased differentiation among microbial communities in different genetic horizons.

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.

References (59)

  • B.F. Rogers et al.

    Temporal analysis of the soil microbial community along a toposequence in Pineland soils

    Soil Biol. Biochem.

    (2001)
  • M.V. Semenov et al.

    Distribution of prokaryotic communities throughout the Chernozem profiles under different land uses for over a century

    Appl. Soil Ecol.

    (2018)
  • M. Šourková et al.

    Soil development and properties of microbial biomass succession in reclaimed post mining sites near Sokolov (Czech Republic) and near Cottbus (Germany)

    Geoderma

    (2005)
  • E.V. Abakumov

    Chronology of ontogenesis of primary soils: review of the problem

    Vestn. Sankt-Pterburrgskogo Univ.

    (2011)
  • E. Abakumov et al.

    Humic acid characteristics in podzol soil chronosequence

    Chem. Ecol.

    (2010)
  • E. Abakumov et al.

    Changes of key biological and chemical properties of soils during the Podzol Formation Process on different aged coastal bars of Ladoga Lake, Russia

    EGU General Assembly 2019, Vienna, Austria, Apr. 7-12, 2019]. In EGU General Assembly 2019 (eds.), Geophysical Research Abstracts, 21

    (2019)
  • A.L. Aleksandrovsky et al.

    New data on the transgression of the Ladoga Lake, the formation of the Neva River and the agricultural development of the northwest of Russia

    Reports of the Academy of Sciences

    (2009)
  • A.L. Alexandrovsky et al.

    Pedogenetic features of habitation deposits in ancient towns of european russia and their alteration under different natural conditions

    Bol. la Soc. Geol. Mex.

    (2012)
  • S.T. Bates et al.

    Examining the global distribution of dominant archaeal populations in soil

    ISME J.

    (2010)
  • A.M. Bolger et al.

    Trimmomatic: A flexible trimmer for Illumina sequence data

    Bioinformatics

    (2014)
  • J.G. Caporaso et al.

    Correspondence QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing

    Nat. Publ. Gr.

    (2010)
  • C. Cerli et al.

    Soil organic matter changes in a spruce chronosequence on Swedish former agricultural soil: I. Carbon and lignin dynamics

    Soil Sci.

    (2006)
  • T.I. Chernov et al.

    Profile analysis of microbiomes in soils of solonetz complex in the Caspian Lowland

    Eurasian Soil Sci.

    (2017)
  • E.L. Chirak et al.

    Taxonomic structure of microbial association in different soils investigated by high-throughput sequencing of 16s-rRNA gene library

    Sel’skokhozyaistvennaya Biol

    (2013)
  • E.K. Costello et al.

    Microbial diversity in alpine tundra wet meadow soil: Novel Chloroflexi from a cold, water-saturated environment

    Environ. Microbiol.

    (2006)
  • M. Delgado-Baquerizo et al.

    A global atlas of the dominant bacteria found in soil

    Science

    (2018)
  • T.Z. DeSantis et al.

    Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB

    Appl. Environ. Microbiol.

    (2006)
  • G. Dobrovolskyi et al.

    Geographya pochv

    (2004)
  • D. Fall et al.

    The efficiency and competitiveness of three Mesorhizobium sp. strains nodulating Acacia senegal (L.) Willd. under water deficiency conditions in the greenhouse

    Symbiosis

    (2011)
  • Cited by (11)

    • Microbial communities in the diagnostic horizons of agricultural Isohumosols in northeast China reflect their soil classification

      2022, Catena
      Citation Excerpt :

      In addition, several large-scale studies also showed that the differences in microbial communities within individual soil profile are equivalent to the variations in the surface horizons across a wide range of biome types (Eilers et al., 2012; Chu et al., 2016). These findings have attracted increasing attention on the deep soil layers in recent years (Eilers et al., 2012; Ivanova et al., 2020). The total microbial biomass in the subsurface horizons (>25 cm) contains up to 35–60% of the whole soil profile in most soil environments (Fierer et al., 2003; Koven et al., 2015; Wu et al., 2022).

    • Geochemical characteristics control potential microbial activity in exposed Late Quaternary alluvial deposits

      2021, Pedobiologia
      Citation Excerpt :

      The majority of studies on the microbial ecology of river basins have focused mainly on topsoils and the horizontal distribution of microbial parameters as well as their interlinkage with environmental factors (Sinsabaugh and Findlay, 1995; Wang et al., 2016). A few studies have assessed relationships among different geochemical and microbial parameters among vertical layers in various buried (unexposed) subsurface soils and in sediments profiles that represent a long depositional period (Turner et al., 2014; Hong et al., 2019; Ivanova et al., 2020). Microbial activities involved in biogeochemical cycling may also be structured by depth in buried soils or sediments due to depth dependent factors such as redox status, availability of oxygen, and light (Fierer et al., 2003; Li et al., 2019).

    View all citing articles on Scopus
    View full text