The modern age of metagenomics has delivered unprecedented volumes of data describing the genetic and metabolic diversity of bacterial communities, but it has failed to provide information about coincident cellular morphologies. Much like metabolic and biosynthetic capabilities, morphology comprises a critical component of bacterial fitness, molded by natural selection into the many elaborate shapes observed across the bacterial domain. In this essay, we discuss the diversity of bacterial morphology and its implications for understanding both the mechanistic and the adaptive basis of morphogenesis. We consider how best to leverage genomic data and recent experimental developments in order to advance our understanding of bacterial shape and its functional importance.

Bacteria come in a wide variety of shapes and sizes. The true picture of bacterial morphological diversity is likely skewed due to an experimental focus on pathogens and industrially relevant organisms. Indeed, most of the work elucidating the genes and molecular processes involved in maintaining bacterial morphology has been limited to rod- or coccal-shaped model systems. The mechanisms of shape evolution, the molecular processes underlying diverse shapes and growth modes, and how individual cells can dynamically modulate their shape are just beginning to be revealed. Here we discuss recent work aimed at advancing our knowledge of shape diversity and uncovering the molecular basis for shape generation in noncanonical and morphologically complex bacteria.

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How Darwin’s “endless forms most beautiful” have evolved remains one of the most exciting questions in biology. The significant variety of bacterial shapes is most likely due to the specific advantages they confer with respect to the diverse environments they occupy. While our understanding of the mechanisms generating relatively simple shapes has improved tremendously in the last few years, the molecular mechanisms underlying the generation of complex shapes and the evolution of shape diversity are largely unknown. The emerging field of bacterial evolutionary cell biology provides a novel strategy to answer this question in a comparative phylogenetic framework. This relatively novel approach provides hypotheses and insights into cell biological mechanisms, such as morphogenesis, and their evolution that would have been difficult to obtain by studying only model organisms. We discuss the necessary steps, challenges, and impact of integrating “evolutionary thinking” into bacterial cell biology in the genomic era.

17Bacteria come in an array of shapes and sizes, but the mechanisms underlying diverse 18 morphologies are poorly understood. The peptidoglycan (PG) cell wall is the primary 19 determinant of cell shape. At the molecular level, much of the studied morphological 20 variation results from the regulation of PG synthesis enzymes involved in elongation 21 and division. These enzymes are spatially controlled by cytoskeletal scaffolding 22 hydrolase. How then does a non-cytoskeletal protein, SpmX, define and constrain PG 30 synthesis to form stalks? Here we report that SpmX and the bactofilin BacA act in 31 concert to regulate stalk synthesis in Asticcacaulis biprosthecum. We show that SpmX 32 acts to recruit BacA to the site of stalk synthesis. BacA then serves as a stalk-specific 33 topological organizer that anchors the PG synthesis complex, including its recruiter 34 SpmX, to the base of the stalk, where stalk PG synthesis occurs. In the absence of 35BacA, cells produce "pseudostalks" that are the result of unconstrained PG synthesis 36 correlated with the mislocalization of SpmX. Finally, we show that BacA is required to 37 inhibit the default function of PG synthesis machinery in cell elongation/division and to 38 prevent DNA entry at the site of stalk synthesis defined by SpmX. Therefore, the protein 39 responsible for recruitment of a morphogenic PG remodeling complex is uncoupled from 40 the protein that topologically organizes the complex. 41 42 to play a role in nutrient uptake [8, 9]. Stalk synthesis requires PG synthesis in a 60 spatially constrained zone in order to extend a thin cylindrical projection of the cell 61 envelope. The stalk is compartmentalized from the cytoplasm, as it is devoid of DNA 62 and ribosomes and excludes even small cytoplasmic proteins such as GFP [9]. 63Asticcacaulis biprosthecum, a gram negative Alphaproteobacterium from the 64 Caulobacteraceae family [10], produces two bilateral stalks whose synthesis depends 65 on PG synthesis at the base of the incipient stalk structures (red arrows in Figure 1A) 66 4 [11]. How do cells harness PG synthesis machinery to produce stalks while preventing 67 its typical function of cell elongation or division? 68 Here we report how a recently identified class of bacterial cytoskeletal protein, known as 69 "bactofilin", plays a dual role by defining the topography of PG synthesis for the 70 synthesis of stalks and by inhibiting a default cell elongation mode at that same site in 71 A. biprosthecum. Bactofilins are conserved throughout the bacterial kingdom and are 72 characterized by the presence of a central conserved DUF583 (or "bactofilin") domain 73 flanked by N-and C-terminal regions of variable length and sequence (Figure 1B) [12]. 74Bactofilins are involved in cell shape determination in a number of species. For 75 example, in the helical Helicobacter pylori and Leptospira biflexa, bactofilins are 76 required for proper helical shape generation [13, 14]. In Caulobacter crescentus, 77 bactofilins optimize the rate of stalk synthesis at the ce...