Elsevier

Soil Biology and Biochemistry

Volume 103, December 2016, Pages 320-326
Soil Biology and Biochemistry

Review Paper
Too much or not enough: Reflection on two contrasting perspectives on soil biodiversity

https://doi.org/10.1016/j.soilbio.2016.09.008Get rights and content

Highlights

  • Two contrasting perspectives are identified in the literature on soil biodiversity.

  • The first ignores the physico-chemical environments of microorganisms.

  • The second assumes that what is true for bacteria also applies to other organisms.

  • Interdisciplinary research is crucial to grasp biodiversity in all its complexity.

Abstract

Soil biodiversity has become a major area of research over the last decade, and the literature on the topic has expanded tremendously in recent years, so much so that a huge number of publications now deal with soil biodiversity every year. This article does not attempt the formidable task of drawing a general picture of where the field is at the moment, but it zeroes in instead on two perspectives that seem to have gathered momentum over time and raise concern about future progress. The first perspective involves the implicit assumption that to make sense of either the species-, genetic-, or functional biodiversity of soils, it is not necessary to consider in detail the features of (micro)habitats provided by soils to organisms, and that analysis of the information provided by extracted DNA or RNA suffices. The second perspective is associated with research on the effect of the physical and chemical characteristics of microhabitats on the activity of microorganisms. It basically hypothesizes that all microorganisms behave similarly, and therefore that observations made mostly with bacteria can be extended readily to all organisms, ignoring taxonomic biodiversity. To illustrate both perspectives, we provide a number of illustrative examples from the relevant literature and analyze them briefly. We argue that these two perspectives, if they spread, will hinder progress in our understanding of soil biodiversity at any level, and especially of its impact on soil processes. In order to return to a more fruitful middle ground, where both a variety of organisms and the characteristics of the microhabitats where they reside are carefully considered, several routes can be envisaged, but our experience suggests that an emphasis on genuinely interdisciplinary research is crucial.

Introduction

Over the last few years, biodiversity has become the object of great interest in the public at large. Soil biodiversity has ridden on the coattails of this surge of attention. Articles in newspapers or in magazines targeting wide audiences frequently mention the billion or so organisms, including many thousands of bacterial and fungal species, that one can find in a single spoonful of soil (e.g., Carson et al., 2010, Delmont et al., 2014), or the fact that there is supposedly more diversity in a gram of soil than above ground in the whole of the Amazon basin. In terms of research, soil biodiversity has become a major area of activity, at different levels: taxonomic, genetic or functional. Among researchers, soil biodiversity has been advocated by some as a critical factor controlling the vast array of microbial processes that are crucial to the proper functioning of soils (Bradford et al., 2014a, Bradford et al., 2014b; Byrnes et al., 2014, Bardgett and van der Putten, 2014, Orgiazzi et al., 2015), regulate their ability to provide services to human populations (Nannipieri et al., 2003), and stabilize global life conditions on earth (Ferris and Tuomisto, 2015). The number of scientific articles devoted to soil biodiversity in soil-, microbiology-, or ecology journals is increasing exponentially, with close to 5000 articles published on the topic just in the last 5 years in the journals indexed in the Web of Science, and the number (1170) of articles devoted to it in 2015 in these same journals representing a 21% increase relative to 2014. At frequent intervals, workshops and conferences are focused on this area all over the world.

The shear mass of publications on soil biodiversity makes the topic very difficult to review in detail. Nevertheless, in broad terms, it is clear that this intense activity has led to important breakthroughs in a number of areas, especially since the development and adoption by soil scientists of a very sophisticated molecular toolbox, including high-throughput sequencing (HTS) technologies. As pointed out by Dini-Andreote and van Elsas (2013), these tools have made it possible to access thousands to millions of microbial phylotypes at relatively low cost and effort. As a result, some aspects of the taxonomic and genetic diversity of rhizosphere and soil microbial communities have progressed appreciably in the last few years (Gattinger et al., 2002, Kondorosi et al., 2013; Grattepanche et al., 2014). Our understanding of the relationship between diversity and functions has also improved markedly, for example with regard to interactions among bacteria (Lupatini et al., 2014) or the symbiotic activity of mycorhizae (Kisa et al., 2007, Martin et al., 2008). In other respects, advances have been appreciable as well but somewhat slower, e.g., on the relationship between biodiversity and fate of soil organic matter under changing environmental conditions, or in terms of understanding how the hydric regime of soils influences their microbial ecology as well as a number of microbial processes, like greenhouse gas release (Blagodatsky and Smith, 2012, Rabot et al., 2014).

Given this recent progress, it would be reasonable to expect that, in the years ahead, there will be a dramatic increase in our ability to characterize the taxonomic-, genetic-, or functional diversity of soil microorganisms, and in our collective understanding of their practical relevance for a wide range of processes about which major questions remain. However, two perspectives that, at least to us, seem to have gained increasing numbers of adherents in recent years, raise concern about the speed with which one can expect this further insight to emerge, and about whether it will be such as to enable researchers to resolve some of the pending issues.

In this context, the key objective of this short review is to identify and describe these two perspectives, as well as to illustrate them with recent publications. Whereas a single illustrative publication would probably have sufficed, we have instead selected two publications for the first perspective, and four for the second, in part to avoid giving the (mistaken) impression that we are singling out a particular publication, which would be unfair to the authors. The book and articles that we have chosen are all very well written and easy to read, with the consequence that it is straightforward to grasp the viewpoint adopted by their authors. After an analysis of these examples, we outline and discuss what we think is needed in order to avoid the potential pitfalls associated with the two perspectives, and to point out what we are convinced is a more fruitful middle ground.

Section snippets

Diverse, but it matters where they live

The first perspective is associated with research that is so focused on biodiversity that most other aspects of soils, and in particular the characteristics of the microscale environments in which soil organisms live, recede into the distant background, when they are mentioned at all. Increasing numbers of articles concentrate on extracting DNA or RNA from soils, and on applying to the extracts a battery of ever more sophisticated molecular biology techniques to characterize the biodiversity of

Forgetting fungi, archaea, protists, and all the others

The second perspective we identify in the literature, in which soil biodiversity is not paid sufficient attention, goes exactly in the opposite direction. Articles associated with this perspective typically deal with processes that either are influenced in some way by soil organisms, or directly influence their activity. In either case, the articles envisage only one type of soil organism, e.g., specific bacterial or fungal species. That, in itself, is not a problem as long as the conclusions

Removing disciplinary blinders

Whether they correspond to situations where the physicochemical characteristics of soils are ignored (first perspective) or where only a subset of organisms present in soils are considered (second perspective), the extreme simplifications of a complex reality, to which the above examples amount, can no doubt be rationalized in a number of different ways, for example by invoking the need to start with simple descriptions of systems, which can later be made more realistic. One of the reviewers of

How do we get to the middle-ground?

Regardless of the specific reasons that have caused interdisciplinarity to be short-changed so far in the examples described earlier, and of what could/should have been done to enable the disciplinary divide to be effectively bridged, we believe that if the two perspectives we have identified continue to attract adherents, we shall end up with masses of experimental information and theories about soil biodiversity that are so fragmentary and incomplete as to be difficult to use for any

Acknowledgments

Sincere gratitude is expressed to two anonymous reviewers for the wealth of insightful comments they provided on the original version of this article.

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