Describing difficult-to-culture bacteria: Taking a shortcut or investing time to discover something new?

Hunting for representatives of as-yet-uncultivated or poorly studied phylogenetic groups of prokaryotes is one of the challenging and highly exciting directions in microbiological research (Zengler et al., 2002, Stevenson et al., 2004; Giovannoni, Stingl, 2007; Dedysh, 2011, Pham and Kim, 2012, Overmann et al., 2017, Thrash, 2019, Lewis et al., 2021). The primary goal of this research is to uncover the phenotypic, metabolic, and functional characteristics of microorganisms that are abundant in nature but, due to some as-yet-unknown specifics of their biology, escape our isolation efforts. Another important goal is to fill in the gaps in the current taxonomic system of prokaryotes by assigning cultured representatives to the taxa whose names were earlier published under the SeqCode, thus enabling testing of properties predicted from genomes, providing resources for biochemistry, biotechnology, and other related microbial sciences (Hedlund et al., 2022).

The efforts in culturing new microbes are nowadays strongly supported by the availability of metagenome- or metatranscriptome-derived data (Bryant et al., 2007, Bomar et al., 2011; Tank, Bryant, 2015a; Wurch et al., 2016; Gutleben et al., 2018; Jiao et al., 2020, Kim et al., 2021, Liu et al., 2022) and are navigated by various molecular tools developed for specific detection of target microorganisms. In other cases, isolation of novel microbes is the result of high-throughput cultivation campaigns (Rappe et al., 2002, Sait et al., 2002, Joseph et al., 2003, Sangwan et al., 2005, Davis et al., 2011, Zeng et al., 2014, Pascual et al., 2016, Henson et al., 2020, Wiegand et al., 2020). Finally, in some rare cases, this is simply an unexpected result of a cultivation-based study (Dunfield et al., 2007, Islam et al., 2008, Tveit et al., 2019). Whatever the isolation history, availability of the desired cultured microorganism opens a possibility of its genome sequencing, comprehensive characterization, and taxonomic description. In practice, however, only some of these possibilities became explored, and many isolates from poorly characterized bacterial phyla never receive an official taxonomic status. This happens because these fastidious microbes are difficult objects for taxonomic studies. In most cases, these isolates are slow-growing microorganisms, which tend to grow under static conditions, do not develop on standard agar media, form large cell clamps in liquid media or, vice versa, grow up to low cell densities only. Many routine laboratory tests, which were originally developed for fast-growing and fast-responding microorganisms, are not fully suitable for slow-growing bacteria. Given also severe problems in depositing difficult-to-handle isolates in culture collections, the time required for describing each of these fastidious bacteria is commonly measured in years. Yet, this work is highly rewarding, since each description of a novel cultivated representative of poorly studied or as-yet-uncultivated phylum immediately becomes a focus of attention. Many taxonomic descriptions of bacteria from enigmatic phyla, however, leave the reader somewhat discouraged since the reported set of characteristics does not differ much from those in bacteria from well-characterized phylogenetic groups. This happens because the authors use routine tests and follow a common practice of preparing taxonomic descriptions that report a minimal set of features to name a newly isolated organism. This practice makes taxonomy unattractive for young microbiologists and deepens a gap between taxonomists and microbial ecologists, who see little value of systematics in interpreting results of environmental molecular diversity studies.

This review was written with a purpose to demonstrate that investing time in detailed analysis of cell biology and experimental verification of genome-encoded capabilities of a newly isolated microorganism opens a window for novel, unexpected findings, which may shape our ideas about the functional role of this microbe in the environment. Some high-quality studies may even revise certain old paradigms. Table 1 was assembled to navigate efforts in preparing taxonomic descriptions that would be of interest to a wide audience of scientists. Major recommendations provided in this table are discussed below and illustrated with some examples. Given the author field of expertise, most examples included in this review address members of the Acidobacteriota and Planctomycetota, the two cosmopolitan and highly diverse bacterial phyla that contain only a limited number of taxonomically characterized organisms.

Comments (0)

No login
gif