Carbon isotopic signatures of microbial trophic levels: insights from microbial mats

Abstract

Microbial mat environments were likely widespread during the Proterozoic and early Paleozoic. As such, interpreting the carbon isotopic compositions (δ13C) of well-preserved organic matter from Proterozoic sediments requires understanding the isotopic consequences of carbon transfer within microbial mats specifically. In modern ecosystems, the δ13C ratios of consumers generally conform to the principle “you are what you eat, +1‰.” However microbial mats, with complex diversity yet few taxa capable of phagocytosis, are not easily classified by canonical ecosystem methods. The primary goal of this thesis was to determine whether “you are what you eat, +1‰” applies to microbial heterotrophy. I use two modern microbial mat environments as analogues for ancient microbially-dominated ecosystems: a subaerial, oxygenated and highly photic environment (Chocolate Pots Hot Springs, Yellowstone National Park, USA; Chapter 2) and a submerged, low-oxygen and benthic environment (Middle Island Sinkhole, Lake Huron, USA; Chapter 3). In both instances, I used Protein Stable Isotope Fingerprinting (P-SIF) to measure the δ13C values of whole proteins separated from natural mat samples and classify the same proteins taxonomically via proteomics. In Chapter 2, we found that Cyanobacteria, obligate heterotrophs, and the monosaccharide moieties from exopolysaccharide (EPS) had indistinguishable δ13C signatures. From these data, we concluded that 1) producers and consumers in this system were sharing primary photosynthate as a common resource, and 2) Cyanobacteria were allocating most of their fixed carbon to exopolysaccharides. In Chapter 3, we found that Cyanobacteria (autotrophs), sulfate reducing bacteria (heterotrophs) and sulfur oxidizing bacteria (autotrophs or mixotrophs), as well as the pentose and hexose moieties of EPS, were all isotopically heterogenous. We hypothesize that these isotopic patterns reflect cyanobacterial metabolic pathways that are relatively more active in low oxygen rather than oxygenated mat environments, resulting in isotopically more heterogeneous C sources in low oxygen mats. In Chapter 4, I use data compiled from the literature to evaluate a potential explanation for the isotopic patterns observed in chapters 2 and 3: that there is a kinetic isotope effect during exopolysaccharide synthesis in Cyanobacteria. Taken as a whole, this thesis cautions against applying “you are what you eat, +1‰” to microbial community food webs, as the δ13C composition of microbial biomass is more closely tied to specific metabolites than to autotrophy versus heterotrophy. As such, interpretations of the δ13C values in sediments derived from predominantly microbial ecosystems should be developed relative to the δ13C values of specific molecular-level carbon sources.