Bacteria as Modular Organisms

Bacteria range in complexity from unicellular rods and cocci (the typical ‘textbook’ bacteria) of more-or-less spherical and occasionally pleomorphic shape, to multicellular, branched (the actinomycetes), or unbranched (e.g., Leucothrix) filaments (Young 2006; Zinder and Dworkin 2013). Some filamentous forms may show gliding motility or are enclosed by a sheath. The myxobacteria (Chaps. 4 and 7; Dworkin 1985) are typically unicellular rods that aggregate and produce ornate fruiting bodies, usually containing specialized resting cells. Despite occasional complex morphology, developmental cycles, or aggregation patterns, all bacterial types can be resolved essentially into growth patterns based on either the unicell or a filamentous unit.

Bacteria may exist in nature as single cells (as in bloodstream infections, septicemia), but apparently this is unusual (Shapiro 1985, 1998). Microcolonies (aggregations visible by light microscopy) form when cell division is not followed by separation of the daughters and dispersal. As early as 1949, Winogradsky was examining such cellular consortia on soil particles, which he termed “families”. They have since been observed in many other habitats including the surfaces of plants and animals; the mucosal walls of the colon; dental plaque; and as suspended particulate matter in lakes and oceans.

The form of a microcolony is affected by the way a cell divides and the nature of its surface. Macroscopically visible colonies of the sort typifying growth in a petri dish are relatively uncommon in nature (Carlile 1980; Pfennig 1989). Conspicuous exceptions are the massive growths in sulfur hot springs, or occasionally in stagnant water (e.g., Pfennig 1989). Where moisture and free water are present at surfaces, structurally complex and typically multispecies biofilms form (Hall-Stoodley et al. 2004; Raaijmakers and Mazzola 2012; Drescher et al. 2016). Indeed, many such multicellular aggregations of bacteria are not grossly dissimilar visually from colonies of fungi, lichens, and bryozoans (Andrews 1998).

Because bacteria tend to form clumps, for the most part they function ecologically as multicells. The disadvantage of this state of affairs for the bacterial cell is largely one of intraspecific competitions for space and nutrients; however, the advantages may include enhanced return from concerted activity (e.g., migration in the case of gliding bacteria or collective enzymatic degradation), or the resistance of pathogenic microbes to host defense mechanisms (phagocytosis; antibodies) and of free-living species to abiotic factors (desiccation; UV light; mechanical erosion). As cell division continues, the clonal aggregation will fragment periodically under the influence of various erosive and dispersal mechanisms. The bacterial equivalent of the genet is thereby dispersed and this asexual process is directly analogous to the shedding of plantlets by various floating aquatic plants such as Lemna, Azolla, and Salvinia, noted earlier. Some bacterial clones are distributed across continents or even globally and may be genetically intact as lineages over hundreds or thousands of years (Spratt and Maiden 1999; Tibayrenc and Ayala 2012).

Given the above levels of organization of a bacterial genet, conceptually it is possible to extend the modular framework to bacteria as organisms. The basic module of a colony of unicells is thus the individual bacterial cell, with successively higher units being microcolonies and macrocolonies and clonal aggregations. The bacterial cell qualifies as the module, whereas the individual cell of unitary organisms does not, because it is iterated indefinitely. Although cell number in unitary organisms changes (e.g., in response to disease; by regular turnover as in replacement of blood and epidermal cells), the number is defined within fairly tight limits by intrinsic genetic and developmental factors. By convention, the term module in eukaryotes is reserved for multicellular structures; while its use in the bacterial context is thus strictly a departure, the relationship of a single cell to the bacterial clone with that, say, of a multicellular Salvinia plantlet to the Salvinia clone is analogous.

Why should one bother including microorganisms in the modular paradigm? The most important reason is that to understand their biology in the real world, we need to consider these organisms in their entirety—as holistic, evolving genetic entities (albeit typically fragmented), rather than from the customary reductionist focus on the individual cell or local population of cells in a test tube or petri dish. It is the clone that changes, disperses, forms mutualistic or parasitic relationships, causes global pandemics, or becomes locally extinct. Attributes and evolutionary possibilities of modular macroorganisms are also those of these microorganisms and they are distinct from those of unitary organisms.