Chapter Three - Bacterial spores, from ecology to biotechnology

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Abstract

The production of a highly specialized cell structure called a spore is a remarkable example of a survival strategy displayed by bacteria in response to challenging environmental conditions. The detailed analysis and description of the process of sporulation in selected model organisms have generated a solid background to understand the cellular processes leading to the formation of this specialized cell. However, much less is known regarding the ecology of spore-formers. This research gap needs to be filled as the feature of resistance has important implications not only on the survival of spore-formers and their ecology, but also on the use of spores for environmental prospection and biotechnological applications.

Section snippets

The challenge of bacterial survival

The unpredictability of environmental conditions in natural ecosystems represents a constant challenge to survival. In consequence, it is highly likely that during its lifetime, an individual organism will have to withstand conditions that are suboptimal for growth and reproduction. There are different responses to this phenomenon. The reduced metabolic activity that occurs in dormant cells is one of these, and dormancy therefore can allow the reduction of the fitness cost that environmental

Mechanisms of bacterial survival through cell differentiation

Among dormant cell forms, the best studied are endospores, which so far have only been found in Firmicutes. Endospore formation is an example of a sophisticated morphophysiological process of cell differentiation. It involves an asymmetric cell division resulting in two cells with distinct morphologies and functions (spore and mother cell), the engulfment of the pre-spore by the mother cell, and the finally remodeling of this spore within the mother cell (Driks, 2002). Endospores are also an

Investigating spores directly from environmental samples

The previous examples considered bacteria forming spores and cyst-like cells that have been cultured and studied in the laboratory. However, it is also possible to investigate the diversity of highly resistant cells directly from environmental samples. Various culture-dependent studies of endospore-forming Firmicutes have shown an interesting distribution pattern suggesting a mismatch between the ecological optima of species and their environmental detection. For example, the revival of

The sporobiota: Prevalence of spores in the human microbiota

The concept of sporobiota has recently been used to characterize a particular fraction of the human microbiota that shares the characteristic of producing highly resistant endospores, which facilitates transmission of spore-formers between individuals (Tetz & Tetz, 2017). The need for defining this unique fraction is not only the consequence of the dominance of this group within the human microbiome (Browne et al., 2016), but also the unique emerging features related to the presence of highly

Potential spore-formers in other microbiomes

The dominance of putative spore-forming groups, especially Firmicutes, appears to be an overarching feature in the microbiomes of mammals (Mao, Zhang, Liu, & Zhu, 2015; Nelson, 2015). A recent study has suggested that captivity affects the mammalian gut microbiome, with Firmicutes as one of the bacterial phyla changing as a consequence of captivity (McKenzie et al., 2017). These changes can implicate either an increase or a reduction in the abundance of specific groups, and those vary for

Prevalence of spore-formers in environmental samples

Despite their potential for global dispersal, the prevalence of many spore-formers in molecular ecology surveys represents a paradox. An example of this current bias is the environmental detection of the phylum Firmicutes. Firmicutes are the second most abundant bacterial phylum according to previous research based on culture collections as well as whole-genome sequencing (Hugenholtz, 2002). Endospore formers are reported to live in a wide range of environments on Earth's surface and subsurface

Spores and environmental sensing

Dormant bacterial cells have the potential to be highly useful in providing records of past environmental conditions. Paleoecological studies in lake sediments intend to combine physicochemical parameters with biological indicators. Typically, the latter corresponds to organisms producing identifiable fossilized structures (e.g., pollen grains or siliceous or calcareous microfossils) that must remain unaltered in order to be preserved in the sediments and hence be analyzed at different

What do spores tell us about antibiotic resistance?

It has been recently suggested that spore-forming bacteria may play an important role in the evolution and spread of antibiotic resistance, due to their ability to withstand antibiotic treatments and their propensity for dispersal (Bengtsson-Palme, Kristiansson, & Larsson, 2018; Shoemaker & Lennon, 2018; Tetz & Tetz, 2017). Spores and spore-formers are a main component of the human microbiome (Browne et al., 2016) and encompass a wide variety of pathogens and opportunistic pathogens, especially

Plant growth promotion

Different groups of beneficial bacteria in the rhizosphere have positive interactions with plants through the colonization of roots and the promotion of plant growth. These bacteria are commonly known as plant growth promoting rhizobacteria (PGPR). PGPR can enhance plant growth either directly or indirectly. Direct mechanisms include fixation of atmospheric nitrogen, solubilization of inorganic phosphorus (Zaidi & Khan, 2007), production of siderophores (Rajkumar, Ae, Prasad, & Freitas, 2010)

Conclusion

Bacterial spores have been known since the dawn of microbiology. Although still seen largely from the perspective of their importance in disease and human health (especially in the case of endospores), bacterial survival in the form of a highly resistance cellular form is likely to be relevant in other ecosystem processes. The basic understanding of the diversity and ecology of spore-formers has direct applications in a diverse range of fields in biotechnology. Nevertheless, in order to advance

Acknowledgments

The authors acknowledge funding from the Swiss National Science Foundation through grants 31003A_179297 (P.J.), CR32I2_162810 (P.J., T.V.), and P2NEP3_178561 (S.F.); the Novartis Foundation through the FreeNovation program; and the U.S. Department of Energy Biological and Environmental Research Division through a Science Focus Area grant to P.S.C. and P.J. (Grant number KP1601010).

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