Elsevier

Applied Soil Ecology

Volume 167, November 2021, 104047
Applied Soil Ecology

Review
Soil metagenomics in grasslands and forests – A review and bibliometric analysis

https://doi.org/10.1016/j.apsoil.2021.104047Get rights and content

Abstract

Metagenomics methods enable the determination of the microbial community found in an environment, and the study of microbial diversity and function. These techniques accelerated the study of the soil microbiome, an important component for global nutrient cycling in diverse ecosystems, including forests and grasslands. We performed a review and bibliometric analysis based on scientific studies published between 2000 and 2019, using the online tools provided by Clarivate analysis - Web of Science Core Collection database. We set up to identify research trends revolving around soil metagenomics in forest and grassland ecosystems, particularly those related with management regimes. Our results showed a rapid growth in the number of papers and a growing interest among the scientific community. Diversity of soil microbial communities was the prime subject addressed for both ecosystems. In top papers, commercial kit extraction methods were preferred, the main NGS technique was pyrosequencing, with Illumina systems gaining traction in the last decade, and bacterial communities were the most studied. This field of research showed a higher average number of citations per paper than related research topics, such as microbiology or environment/ecology. Understanding functional diversity and the ecological and applied potential of soil microbiomes is one of the current trends in soil metagenomics studies.

Introduction

Soil is responsible for fundamental services, including nutrient cycling, transformation of organic materials and toxic compounds, water regulation and control of pests and diseases (Dominati et al., 2010; Smith et al., 2015). Soil microbiome is considered fundamental for its role in virtually all soil processes, and growing evidence shows that soil organisms play key roles in a multitude of ecosystem functions (Wagg et al., 2014a; Fierer, 2017). The sustainability of production in agricultural land is, at a large scale, the result of microbial composition, abundance, and activity (de Vries et al., 2013; Bradford et al., 2014; Pellkofer et al., 2016; Wagg et al., 2018). For instance, the abundance of soil microbes can be associated with the soil's capacity to sequestrate carbon and its ability to maintain the ecosystem functions under climate change (Zhou et al., 2012). Furthermore, it plays an important role in nutrient cycling, with P-solubilizing microorganisms and arbuscular mycorrhizal fungi being of extreme importance in agroecosystems (Hallama et al., 2019). Moreover, the abundance of soil microbes has also been linked with aboveground diversity (Wagg et al., 2014b; Legay et al., 2016; Wang et al., 2019). Notwithstanding, although there is a consensus among the scientific community about the importance of soil biodiversity, this has not been broadly translated into policymaking and general public awareness, with few countries having legislation or specific policies targeting soil biodiversity and sustainable soil management. Nevertheless, there seems to exist an increasing concern to promote sustainable soil management practices, especially in agricultural systems (UN, 2020). Furthermore, a deep understanding of soil bacterial and fungal communities and of the processes that affect soil fertility (Carbonetto et al., 2014; Foo et al., 2017), will allow their management to stimulate the presence of beneficial species and avoid the spread of detrimental ones (Chaparro et al., 2012; Panelli et al., 2017; Pineda et al., 2019).

Until recently, even though soil is an important component of global ecosystems, little was known about biodiversity patterns, the interactions in the belowground section of terrestrial ecosystems, and how they function in nature (Bardgett and van der Putten, 2014; Andriuzzi and Wall, 2017; Bardgett, 2018). Moreover, most soil microbial taxa remain undescribed (Ramirez et al., 2014; Walsh et al., 2019; Oliverio et al., 2020). The advent of metagenomics, whose ultimate objective is the study of organisms in their communities, provided the possibility of studying microorganisms that are not cultivable in a laboratory environment, opening the doors to explore most of the microbial communities present in environmental samples, including soil (Garrido-Cardenas and Manzano-Agugliaro, 2017). Additionally, the creation of databases such as SILVA (https://arb-silva.de/) allowed for the identification of microorganisms with up-to-date quality-controlled aligned ribosomal RNA gene sequences from the Bacteria, Archaea and Eukaryota domains (Yilmaz et al., 2014). Until the beginning of this decade, most metagenomic studies had a focus on agriculture and food but by 2016, its application in medicine, immunology, microbiology, biochemistry, genetics and molecular biology had surpassed its use in agriculture and ecology (Garrido-Cardenas and Manzano-Agugliaro, 2017), with much still to be learned regarding soil microbial communities. To surpass this lack of knowledge, several efforts have been conducted such as the Earth Microbiome Project (Gilbert et al., 2014), the LUCAS project (Fernández-Ugald et al., 2016) and the International Decade of Soils that was launched in 2015 by the International Union of Soil Sciences (iuss.org). These efforts resulted in a rapid increase in the number of scientific publications, making it gradually impracticable to stay current with all the lines of research being published. Moreover, and unlike the examples cited above, many research lines focused on empirical contributions, meaning that most of the publications corresponded to fragmented research (Briner and Denyer, 2012). This fragmentation hinders the ability to gather knowledge from actively accumulated evidence, through a collection of previous research papers. Thus, to keep up with the large amount of research published every year, literature reviews are increasingly assuming a crucial role (Ellegaard and Wallin, 2015; Mao et al., 2018; Chen et al., 2019a; Liu et al., 2019), as they synthesize past findings, allowing to use the current knowledge base to advance research, and providing evidence-based understanding which in turn sustain professional judgment and expertise (Rousseau, 2012). In the topic of metagenomics, Garrido-Cardenas and Manzano-Agugliaro (2017) performed a bibliometric analysis regarding the worldwide evolution of metagenomics research while, in the same year, Fierer published a review on the complexities of soil microbiomes; and in 2020, Jansson and Hofmockel delved into the existing knowledge regarding the impacts of climate change on soil microorganisms, while Kim et al. presented a meta-analysis on the effects of cover crops on soil microbiome.

Following alterations in the spatial distribution of potential vegetation types, emerging according to climate zones (i.e., biomes), due to climate change and the expansion of anthromes (i.e., anthropogenic biomes), many areas were altered into rangeland or pastureland, which globally became one of the dominant land cover types (Song et al., 2018). Meanwhile, the need to reduce greenhouse emissions from cattle grazing is demanding more efficient and sustainable production practices in grasslands around the world (Busby et al., 2017; Dini et al., 2017; Ribeiro-Filho et al., 2020). On the other hand, forests have a key role in carbon sequestration (Huang et al., 2020), above and belowground, even though natural, or primordial forests have been progressively replaced by planted or secondary forests worldwide (Sloan and Sayer, 2015). Nevertheless, forests still play a key role in preserving soil quality and in mitigating erosion (Altieri et al., 2018). Moreover, forests have been used as baseline ecosystems in many studies addressing changes in soil quality and ecology, in agriculture and other types of human-dependent production systems (Navarrete et al., 2015; Tripathi et al., 2016). Furthermore, in the beginning of the century, globally, about 2.955 Mha were occupied by pastureland and 3.678 Mha by forest (3.507 natural and 170.5 Mha planted, Lambin and Meyfroidt, 2011). In this context, researchers have been particularly interested in analysing changes in plant, and more recently in soil microbial diversity, along gradients of management intensity in grasslands and forests. The metagenomic approach has an enormous potential in the study of these two parallel systems. This review and bibliometric analysis intend to assess the publication trends in metagenomics studies dedicated to microbial soil communities, with an emphasis on grassland/pastureland and forest ecosystems, spanning from its origins in the beginning of the century until the year 2019.

Section snippets

Data sources and tools

Bibliometrics uses a range of methods to analyse the scientific literature quantitatively and to evaluate the relative importance of scientific production in a specific field (Montoya et al., 2016). This methodology delivers a very useful tool to comprehend the evolution of research and foresee the future of a given topic (Cañas-Guerrero et al., 2013; Singh et al., 2014).

The data for this bibliometric study was collected from the Web of Science Core Collection (WoSCC). The WoSCC database is a

Metagenomics and soil

From 2000 to 2019, 13,543 papers written in English were retrieved from WoS for the broader metagenomics search. As expected, the top category was Microbiology (4255 papers, 29%) (Fig. 2). By adding the keyword “soil”, our search obtained 2212 papers related to soils metagenomics, which represented around 16% of the total of papers retrieved for metagenomics. A difference can be seen in the top categories (Fig. 2), but Microbiology (798 papers) continued to dominate (31%).

The 10 countries that

Discussion

Our data showed a worldwide, consistent increase in the number of papers published between 2000 and 2019 referring to metagenomics, with a total of 13,543. A similar study by Garrido-Cardenas and Manzano-Agugliaro (2017), using the Elsevier Scopus database from 1996 to 2016, and the keywords “metagenomics” and “metagenomic” obtained 9277 results (i.e., a difference of 4266 regarding our study). This could be justified by the differences in temporal scope, database source, and keywords,

Funding

This work was supported by Fundação para a Ciência e Tecnologia (FCT) through Fundo Social Europeu (FSE) and the European Union (grant number SFRH/BD/130307/2017); and by the Azores Government (FRCT) through Project BIOINVENT, BIODIVERSA Program - Generic bio-inventory of functional soil microbial diversity in permanent grassland ecosystems across management and climate gradients.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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