Diverse spatial organization of photosynthetic membranes among purple nonsulfur bacteria

Abstract

24In diverse bacteria, proper cellular physiology requires the utilization of protein-or membrane-25 bound compartments that afford specific metabolic capabilities. One such compartment is the 26 light-harvesting intracytoplasmic membrane (ICM) of purple nonsulfur bacteria (PNSB). Here we 27 reveal that ICMs are subject to differential spatial organization among PNSB. We visualized 28ICMs in live cells of fourteen PNSB species by exploiting the natural autofluorescence of the 29 photosynthetic machinery. We then quantitatively characterized ICM localization using 30 automated computational analysis of autofluorescence patterns within single cells across the 31 population. Our studies revealed that ICMs are localized in distinct subcellular patterns that 32 differ between species; some PNSB elaborate ICMs throughout the cell, while others spatially 33 restrict ICM to varying degrees. The most highly-restricted ICMs were localized in a specific 34 pattern corresponding to progression of cell growth and division. An identical pattern of ICM 35 restriction was conserved across at least two genera. Phylogenetic and phenotypic comparisons 36 established that ICM localization and ICM architecture are not strictly interdependent and that 37 neither trait fully correlates with the evolutionary relatedness of the species. This discovery of 38 new diversity in bacterial cell organization has implications for understanding both the 39 mechanisms underpinning spatial arrangement of bacterial compartments and the potential 40

The development of intracytoplasmic membranes in alphaproteobacteria involves the conserved mitochondrial crista-developing protein Mic60

“…Mic60 and Orf52 have broad phylogenetic distributions that overlap with the distribution of ICMs in the Alphaproteobacteria Prokaryotic homologs of Mic60 have been previously shown to be restricted to alphaproteobacterial species, thus serving as a synapomorphy for the clade that comprises both mitochondria and the Alphaproteobacteria 19,20,2 . Moreover, phylogenetically diverse alphaproteobacteria are known to develop extensive bioenergetic ICMs that house electron transport chains associated with physiological processes such as methanotrophy (methane oxidation), nitrification (nitrite oxidation), and (aerobic or anaerobic) anoxygenic photosynthesis [21][22][23]26,24 . However, it is unclear to what extent the presence of Mic60, which has been hypothesized to be involved in ICM development 26 , correlates with the occurrence of ICMs.…”

“…Mitochondria also compartmentalize other metabolic pathways 1,5 . Because aerobic respiration occurs at internalized membranes that can expand greatly, mitochondria allow for the proportional increase (or linear homologues of Mic60, many alphaproteobacteria also develop either lamellar or vesicular intracytoplasmic membranes (ICMs) that house diverse electron transport chains involved in methanotrophy, nitrification, and anoxygenic photosynthesis [21][22][23][24][25] . This raises the possibility that Mic60 is involved in the development and/or stability of ICMs in alphaproteobacteria, and that mitochondrial cristae evolved from ancestral alphaproteobacterial ICMs 26 .…”

“…After harvesting, the strains were cryopreserved, contrasted, and imaged using transmission electron microscopy (TEM). Randomized TEM micrographs were blindly scored to quantitatively evaluate phenotypes associated to the peripheral stacked lamellar ICMs of R. palustris and the uniformly distributed vesicular ICMs of R. sphaeroides 24 (Fig. 3E-H, Movie S1-4).…”