L-form bacteria, cell walls and the origins of life

Abstract

The peptidoglycan wall is a defining feature of bacterial cells and was probably already present in their last common ancestor. L-forms are bacterial variants that lack a cell wall and divide by a variety of processes involving membrane blebbing, tubulation, vesiculation and fission. Their unusual mode of proliferation provides a model for primitive cells and is reminiscent of recently developed in vitro vesicle reproduction processes. Invention of the cell wall may have underpinned the explosion of bacterial life on the Earth. Later innovations in cell envelope structure, particularly the emergence of the outer membrane of Gram-negative bacteria, possibly in an early endospore former, seem to have spurned further major evolutionary radiations. Comparative studies of bacterial cell envelope structure may help to resolve the early key steps in evolutionary development of the bacterial domain of life.

Figure 1.

Outline phylogenetic tree of the bacteria and the distribution of key cell envelope features. (a) An outline phylogenetic tree for the bacteria, based on the major phylogenetic groups recognized by Wu et al. [3]. The detailed branching order is tentative for reasons outlined in the text. Groups traditionally described as Gram-negative and Gram-positive are indicated in red and blue text, respectively. (b,c) Distribution of genes required for PG (b) or Lipid A (c) synthesis, based on the output from STRING v. 9.0 [4] using murC and lpxC as markers. Similar results were obtained with other genes from the PG or the OM pathways (not shown). The number of organisms in each group are shown. Plus symbols (+) denote greater than 90% of organisms contained a likely gene homologue; plus or minus symbol (±), 50–70%; minus symbol (−), less than 5%. (d) Comments on current knowledge of cell envelope structures of various groups based mainly on information from Bergey's Manual of Systematic Bacteriology [5].

Figure 2.

L-form proliferation and its similarity to in vitro vesicle replication. (a) Schematic of L-form proliferation based on observations with defined primary L-forms of B. subtilis [16] together with the vesiculation described by Dell'Era et al. [17]. (b–d) Comparison of L-form cells and replicating lipid vesicles. (b) A large B. subtilis L-form surrounded by recently generated progeny blebs [15]. (c) L-form-like cells from the urine of a Fanconi patient [18]. (d) In vitro proliferating lipid vesicle [19]. Scale bars: (c) 5 μm and (d,e) 10 μm.

Figure 3.

Pivotal role for the cell wall in the bacterial radiation. (a) Schematic of a primitive cell bounded by a single lipid bilayer. Objects in different colours and shapes represent distinct separately evolving proto-genomes. The cells proliferate by tubulation or blebbing, similarly to L-forms. Such cells would have undergone frequent fusion and fission events, resulting in rampant horizontal gene transfer. The cells would have been fragile and overall growth slow. (b) Invention of an early form of the cell wall would have led to early forms of true bacteria. The presence of the wall would have crystallized the genome from which it was encoded by largely preventing horizontal gene transfer. Polarized growth of the wall would have enhanced the efficiency of growth and division, as well as chromosome replication and segregation. (c) Rapid and efficient growth, together with a tough protective layer would have enabled effective exploration of novel niches and the evolution of many new forms.

Figure 4.

Evolution of the Gram-negative OM via endospore formation. Key steps in the general sporulation process are labelled below. For simplicity, growth and early steps of sporulation of modern Veillonaceae in the diderm state are not shown.

Figure 5.

Revised scheme for the evolutionary divergence of the bacteria. Invention of the PG cell wall resulted in the earliest bacteria with a simple monoderm structure. The evolutionary relationships between modern Firmicutes, Actinobacteria, Chloroflexi and the Deinococcus-Thermus group remain unclear. The major Gram-negative phyla are now suggested to have emerged from within the ancestors of the Firmicutes by retention of the endospore OM. The Tenericutes probably emerged from the same ancient group by complete loss of the wall.