Elsevier

Pedosphere

Volume 32, Issue 1, February 2022, Pages 75-89
Pedosphere

Difficult-to-culture bacteria in the rhizosphere: The underexplored signature microbial groups

https://doi.org/10.1016/S1002-0160(21)60062-0Get rights and content

ABSTRACT

Microorganisms represent a substantial portion of the earth's biodiversity and biomass, and the plant rhizosphere is an innate reservoir teeming with heterogeneous microbes predominated by bacterial communities. Rhizospheric microbial diversity (genetic, phenotypic, and metabolic) has been extensively studied to understand the key ecological roles played by the microbial members, including plant growth promotion. The application of 16S rRNA gene sequencing and next-generation sequencing (NGS) technologies has revolutionized the discovery of novel bacterial groups that have remained undetected by traditional cultivation-based approaches. Such technological advancements have opened new vistas in our current understanding of predominant but concealed and missed bacterial diversity referred to as difficult-to-culture bacterial lineages, especially the predominant phyla Acidobacteria, Verrucomicrobia, Planctomycetes, and Gemmatimonadetes. Regardless of their ubiquity and prevalence, little is known about their ecophysiology because of the non-availability of culturable members. More recently, there has been increased interest in understanding the cosmopolitan distribution and diversity of the difficult-to-culture bacteria, focusing on their role in driving complex plant-microbial interactions and mobilizing nutrients in soil and their potential as sources of novel bioactive metabolites. As an initial step, we review the distribution and significance of such bacterial phyla in soil, their ecophysiological roles, and their hidden plant growth promoting potential. The ability to select and deploy plant probiotic bacteria from the difficult-to-culture fraction of the bacterial community might open new avenues for improving crop health.

Section snippets

INTRODUCTION

Microbial biodiversity in terrestrial ecosystems potentially influences important ecophysiological processes because microbes play crucial roles in driving biogeochemical cycles. Soil harbors a complex microbial consortium with an abundant bacterial population. The complex below-ground plant-bacterial interactions, especially in the rhizosphere, are major determining factors of plant health and soil fertility. Rhizosphere bacteria that benefit plants through nitrogen fixation, phosphate

RHIZOSPHERE MICROBIAL COMMUNITIES

Soil is a complex, dynamic, and diverse environment populated with a plethora of diverse microbes that keep it healthy and productive. Rhizosphere soil is under the direct influence of plant roots and differs considerably from the bulk soil in terms of its physico-biochemical properties (Hinsinger, 1998) and associated microbial communities. The rhizosphere is home to a wide range of prokaryotic and eukaryotic taxa, of which bacteria and fungi comprise the most abundant groups (Buée et al., 2009

MISSED DIVERSITY: THE RARE BIOSPHERE AND MICROBIAL DARK MATTER

Novel or unrecognized bacterial taxa are present in low abundance within a microbial community and constitute the largely unexplored rare biosphere (Sogin et al., 2006; Lynch and Neufled, 2015; Bull and Goodfellow, 2019). Unprecedented access to this rare biosphere has been accomplished with the aid of amplicon-based 16S rRNA gene biodiversity studies, including pyrosequencing (Janssen, 2006; Jones et al., 2009; Shade et al., 2012) and Illumina sequencing (Bartram et al., 2011). Despite its

OVERVIEW OF CULTURE-DEPENDENT AND INDEPENDENT APPROACHES TO STUDY DIFFICULT-TO-CULTURE BACTERIA

Overmann et al. (2017) reviewed the techniques available for culturing difficult-to-culture bacterial phyla and predicted that such underexplored phyla could represent new and innovative research opportunities. Culture-dependent studies revealed that conventional cultivation media favor the growth of fast-growing bacteria, masking the growth of slow growers, including oligotrophs (Koch, 1997; Connon and Giovannoni, 2002); however, the use of dilute nutrient media has been successful in

INSIGHTS INTO THE ECOLOGICAL ROLES OF PREDOMINANT DIFFICULT-TO-CULTURE BACTERIAL PHYLA

Physiologic, genomic, and metagenomic studies provide evidence of the crucial roles played by difficult-to-culture bacterial phyla inhabiting the soil environment. Nutrient cycling is one of the most essential ecological processes in which microorganisms play a crucial role. Determining rhizospheric difficult-to-culture bacterial interactions and their dynamics within soil ecosystems is of high priority from an ecological perspective. The predominant difficult-to-culture bacterial phyla

DIFFICULT-TO-CULTURE BACTERIA AS POTENTIAL PGPR

The difficult-to-culture bacterial taxa have been widely reported from rhizosphere soils, suggesting that they may have PGP abilities (da Rocha et al., 2010a, b). As already stated, free-living soil bacteria that inhabit the rhizosphere and improve overall plant health, leading to augmented plant growth, are referred to as PGPR (Dutta and Podile, 2010; Goswami et al., 2016). The PGPR are considered to be important plant probiotics (Flores-Félix et al., 2015) as they increase crop yields, act as

CONCLUSIONS AND FUTURE CHALLENGES

The varied metabolic and ecophysiological functions of the difficult-to-culture bacterial phyla in soil open the scope to finding the bright side of microbial dark matter. Culture-dependent and -independent approaches together provide a holistic approach to the study of the soil microbial community, especially the difficult-to-culture phyla. As rhizosphere soils are a major reservoir of microbial consortia, more attention sensu stricto should be paid to the rhizospheric difficult-to-culture

CONTRIBUTION OF AUTHORS

Sadaf KALAM and Anirban BASU contributed equally to this work and shared the first authorship.

ACKNOWLEDGEMENTS

This work was supported by the Department of Science and Technology (DST), Government of India (GoI), in the form of DST-WOS-A Women Scientist Fellowship for Sadaf KALAM (Grant no. SR/WOS-A/LS-294/2012(G)) and in the form of J. C. Bose Fellowship for Appa Rao PODILE (Grant no. JCB/2017/000053). We gratefully acknowledge the DST-FIST level II and University Grants Commission Special Assistance Programme (UGC-SAP) support for the Department of Plant Sciences, School of Life Sciences, University

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