Episymbiotic bacterium induces intracellular lipid droplet production in its host bacteria

Abstract

Saccharibacteria (formerly TM7) Nanosynbacter lyticus type strain TM7x exhibits a remarkably compact genome and an extraordinarily small cell size. This obligate epibiotic parasite forms a symbiotic relationship with its bacterial host, Schaalia odontolytica, strain XH001 (formerly Actinomyces odontolyticus strain XH001). Due to its limited genome size, TM7x possesses restrained metabolic capacities, predominantly living on the surface of its bacterial host to sustain this symbiotic lifestyle. To comprehend this intriguing, yet understudied interspecies interaction, a thorough understanding of the physical interaction between TM7x and XH001 is imperative. In this study, we employed super-resolution fluorescence imaging to investigate the physical association between TM7x and XH001. We found that the binding with TM7x led to a substantial alteration in the membrane fluidity of the host bacterium XH001. Unexpectedly, we revealed the formation of intracellular lipid droplets in XH001 when forming episymbiosis with TM7x, a feature not commonly observed in oral bacteria cells. The TM7x-induced LD accumulation in XH001 was further confirmed by label-free non-invasive Raman spectroscopy, which also unveiled additional phenotypical features when XH001 cells are physically associated with TM7x. Further exploration through culturing host bacterium XH001 alone under various stress conditions showed that LD accumulation was a general response to stress. Intriguingly, a survival assay demonstrated that the presence of LDs likely plays a protective role in XH001, enhancing its overall survival under adverse conditions. In conclusion, our study sheds new light on the intricate interaction between Saccharibacteria and its host bacterium, highlighting the potential benefit conferred by TM7x to its host, and further emphasizing the context-dependent nature of symbiotic relationships.

Comparative Lipidomics of Oral Commensal and Opportunistic Bacteria

“…Nanobacter lyticus (TM7x) was included in these analyses since this ultrasmall bacterium (200 to 300 nm), which possesses a Gram-positive cell envelope, survives as an epibiont on the surfaces of larger oral bacteria [67,68] and is present in human saliva [69,70]. Our data are the first lipidomics characterization of this important oral bacteria and demonstrate the major lipid family produced by the more compact genome of this bacteria is glycerol-phosphocholines (Figure 4; Supplementary Tables).…”

“…PE-ceramides are lipid biomarkers of several Gram-negative genera, including terioides, Porphyromonas, Prevotella, Tanneralla, and Parabacteroides [66][67][68][69][70] and are cons ent lipids in insects [71]. PE-ceramides have been monitored in human gingival tiss blood, vascular tissues, and brain [67,73].…”

Identifying essential genes inSchaalia odontolyticausing a highly-saturated transposon library

“…While a number of Saccharibacteria and host pairs have been recently isolated (1)(2)(3)(4), the Nanosynbacter lyticus type strain, TM7x (HMT_952), and Schaalia odontolytica (formerly Actinomyces odontolyticus subsp. actinosynbacter) strain XH001 coculture is the first and most well-studied pair (5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17). Studying their interaction has been stymied due to TM7x's recalcitrance to growth in independent culture and paucity of genetic tools for both species.…”