Carbon isotopic composition of lipid biomarkers from an endoevaporitic gypsum crust microbial mat reveals cycling of mineralized organic carbon

Abstract

Microbial mats that inhabit gypsum deposits in ponds at Guerrero Negro, Baja California Sur, Mexico, developed distinct pigmented horizons that provided an opportunity to examine the fixation and flow of carbon through a trophic structure and, in conjunction with previous phylogenetic analyses, to assess the diagenetic fates of molecular δ13C biosignatures. The δ13C values of individual biomarker lipids, total carbon, and total organic carbon (TOC) were determined for each of the following horizons: tan‐orange (TO) at the surface, green (G), purple (P), and olive‐black (OB) at the bottom. δ13C of individual fatty acids from intact polar lipids (IPFA) in TO were similar to δ13C of dissolved inorganic carbon (DIC) in the overlying water column, indicating limited discrimination by cyanobacteria during CO2 fixation. δ13CTOC of the underlying G was 3‰ greater than that of TO. The most δ13C‐depleted acetogenic lipids in the upper horizons were the cyanobacterial biomarkers C17 n‐alkanes and polyunsaturated fatty acids. Bishomohopanol was 4 to 7‰ enriched, relative to alkanes and intact polar fatty acids (IPFA), respectively. Acyclic C20 isoprenoids were depleted by 14‰ relative to bishomohopanol. Significantly, ∆[δ13CTOC − δ13C∑IPFA] increased from 6.9‰ in TO to 14.7‰ in OB. This major trend might indicate that 13C‐enriched residual organic matter accumulated at depth. The permanently anoxic P horizon was dominated by anoxygenic phototrophs and sulfate‐reducing bacteria. P hosted an active sulfur‐dependent microbial community. IPFA and bishomohopanol were 13C‐depleted relative to upper crust by 7 and 4‰, respectively, and C20 isoprenoids were somewhat 13C‐enriched. Synthesis of alkanes in P was evidenced only by 13C‐depleted n‐octadecane and 8‐methylhexadecane. In OB, the marked increase of total inorganic carbon δ13C (δ13CTIC) of >6‰ perhaps indicated terminal mineralization. This δ13CTIC increase is consistent with degradation of the osmolyte glycine betaine by methylotrophic methanogens and loss of 13C‐depleted methane from the mat.

Absence of canonical trophic levels in a microbial mat

“…It further requires that water‐column remineralization is intense enough to enrich lipids in 13 C while both (1) preserving sufficient heterotrophic lipid to form the majority of the preserved lipid pool and (2) degrading sufficient heterotrophic biomass such that primary biomass forms the majority of the kerogen pool (Close et al, 2011). While such conditions are predicted to occur only rarely, if ever, within the water column (Close et al, 2011), some have suggested that these conditions are possible within microbial mats (Jahnke & des Marais, 2019; Pawlowska et al, 2013).…”

“…To date, a major obstacle in this effort has been measuring taxonomically resolved, natural abundance δ 13 C values for microbial communities at sub‐1‰ resolution. Prior studies comparing the δ 13 C values of phylum‐specific biomarker lipids consistently report measurements at sub‐1‰ resolution (e.g., Jahnke et al, 2004; Jahnke & des Marais, 2019; van der Meer et al, 2003; Werne et al, 2002). However, using these data to estimate the δ 13 C values of autotrophic and heterotrophic microbial biomass is infeasible, given the variable offset in δ 13 C values between lipids and biomass (Blair et al, 1985; DeNiro & Epstein, 1977; Tang et al, 2017).…”

“…To date, a major obstacle in this effort has been measuring taxonomically resolved, natural abundance δ 13 C values for microbial communities at sub-1‰ resolution. Prior studies comparing the δ 13 C values of phylum-specific biomarker lipids consistently report measurements at sub-1‰ resolution (e.g., Jahnke et al, 2004;Jahnke & des Marais, 2019;van der Meer et al, 2003;Werne et al, 2002).…”

Detecting pigments from gypsum endoliths using Raman spectroscopy: From field prospection to laboratory studies

“…These are commonly based on analysing extractable organic compounds or dispersed insoluble kerogen. [52][53][54] In these studies, the information on the relationship between organic matter and mineral matrix is lost. Understanding endoliths including their strategies to cope in more or less harsh environments requires collecting deep information about microbiology, presence of microorganisms in the frame of mineral matrix, distribution of their biomarkers, including their pigments.…”

Messinian bottom‐grown selenitic gypsum: An archive of microbial life

“…Stivaletta & Barbieri, 2009;Stivaletta et al, 2010;Jahnke & Des Marais, 2019;Huang et al, 2020). The low biological diversity of modern hypersaline environments is also mirrored by molecular fossil inventories, mostly reflecting input of lipids from halophilic archaea such as DGDs(Dawson et al, 2012;Grice et al, 1998;Turich & Freeman, 2011) and cyanobacteria such as saturated and monounsaturated heptadecanes and heptadecenes(Jahnke et al, 2014).Compared to most modern marine gypsum occurrences (e.g.,Jahnke et al, 2014), molecular fossils of the studied Messinian gypsum reflect different ecologies.…”