The Chlorobiales are anoxygenic phototrophs that produce solid, extracellular elemental sulfur globules as an intermediate step in the oxidation of sulfide to sulfate. These organisms must export sulfur while preventing cell encrustation during S 0 globule formation; during globule degradation they must find and mobilize the sulfur for intracellular oxidation to sulfate. To understand how the Chlorobiales address these challenges, we characterized the spatial relationships and physical dynamics of Chlorobaculum tepidum cells and S 0 globules by light and electron microscopy. Cba. tepidum commonly formed globules at a distance from cells. Soluble polysulfides detected during globule production may allow for remote nucleation of globules. Polysulfides were also detected during globule degradation, probably produced as an intermediate of sulfur oxidation by attached cells. Polysulfides could feed unattached cells, which made up over 80% of the population and had comparable growth rates to attached cells. Given that S 0 is formed remotely from cells, there is a question as to how cells are able to move toward S 0 in order to attach. Time-lapse microscopy shows that Cba. tepidum is in fact capable of twitching motility, a finding supported by the presence of genes encoding type IV pili. Our results show how Cba. tepidum is able to avoid mineral encrustation and benefit from globule degradation even when not attached. In the environment, Cba. tepidum may also benefit from soluble sulfur species produced by other sulfur-oxidizing or sulfur-reducing bacteria as these organisms interact with its biogenic S 0 globules.
Microbial sulfur metabolism, particularly the formation and consumption of insoluble elemental sulfur (S 0 ), is an important biogeochemical engine that has been harnessed for applications ranging from bioleaching and biomining to remediation of waste streams. Chlorobaculum tepidum, a low-light-adapted photoautolithotrophic sulfur-oxidizing bacterium, oxidizes multiple sulfur species and displays a preference for more reduced electron donors: sulfide > S 0 > thiosulfate. To understand this preference in the context of light energy availability, an "energy landscape" of phototrophic sulfur oxidation was constructed by varying electron donor identity, light flux, and culture duration. Biomass and cellular parameters of C. tepidum cultures grown across this landscape were analyzed. From these data, a correction factor for colorimetric protein assays was developed, enabling more accurate biomass measurements for C. tepidum, as well as other organisms. C. tepidum's bulk amino acid composition correlated with energy landscape parameters, including a tendency toward less energetically expensive amino acids under reduced light flux. This correlation, paired with an observation of increased cell size and storage carbon production under electron-rich growth conditions, suggests that C. tepidum has evolved to cope with changing energy availability by tuning its proteome for energetic efficiency and storing compounds for leaner times. IMPORTANCEHow microbes cope with and adapt to varying energy availability is an important factor in understanding microbial ecology and in designing efficient biotechnological processes. We explored the response of a model phototrophic organism, Chlorobaculum tepidum, across a factorial experimental design that enabled simultaneous variation and analysis of multiple growth conditions, what we term the "energy landscape." C. tepidum biomass composition shifted toward less energetically expensive amino acids at low light levels. This observation provides experimental evidence for evolved efficiencies in microbial proteomes and emphasizes the role that energy flux may play in the adaptive responses of organisms. From a practical standpoint, our data suggest that bulk biomass amino acid composition could provide a simple proxy to monitor and identify energy stress in microbial systems. Microbes that synthesize or degrade insoluble sulfur minerals are instrumental in the biogeochemical sulfur cycle (1) and have been applied for biomining (2, 3) and sulfide remediation (4-7). However, little is known about how these organisms respond to fluctuations in available energy due to shifts in electron donor identity, fixed carbon availability, or light in the case of phototrophic bacteria. A deeper understanding of microbial strategies for coping with energy fluctuations has the potential to improve microbe-catalyzed industrial processes (8) and to impact our understanding of microbial ecology as shaped by energy availability (9). Furthermore, a specific understanding of these adaptations among mic...
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