Rapid sulfurization obscures carotenoid distributions in modern euxinic environments

Abstract

Anoxygenic phototrophic bacteria (green and purple sulfur bacteria) thrive in anoxic environments where light penetrates a sulfide-containing (euxinic) water column. Genomic data and photosynthetic bacterial carotenoid pigments should provide complementary information on the spatio-temporal dynamics of anoxygenic phototrophs in modern euxinic environments. In turn, these contemporary depositional settings often serve as analogues for ancient counterparts. However, in some modern environments, DNA-informed patterns of phototrophic sulfur bacteria occurrence do not match distributions of their carotenoid inventories. One possible explanation for these seemingly incompatible observations is that the rapid sulfurization of carotenoids and incorporation into macromolecules via multiple carbon–sulfur bonds prevents or confounds their detection by conventional means. Here, to evaluate this conundrum, we revisit some representative contemporary euxinic environments where anoxygenic phototrophic bacteria have mostly been detected based on genomic analyses. Although free intact carotenoids are sporadically detected in surface sediments, their distributions do not reveal a complete picture. Exogenously sourced fossil carotenoids (e.g., paleorenieratane) is an additional complication. Carotenoid inventories obtained by desulfurization with Raney nickel, on the other hand, stand in stark contrast to those present as free lipids. In particular, sulfur-linked carotenoids present in euxinic lake sediments provide a more complete picture of compositions of anoxygenic sulfur bacterial communities and account for discrepancies reported in previous studies. We observe a closer alignment between genomic data and patterns of sulfurized carotenoids and, importantly, our results highlight how sulfurization serves as a pathway for the rapid modification of highly functionalised lipids and their sequestration into the macromolecular component of sediment extracts.