Limitation of Microbial Processes at Saturation-Level Salinities in a Microbial Mat Covering a Coastal Salt Flat

Abstract

Hypersaline microbial mats are dense microbial ecosystems capable of performing complete element cycling and are considered analogs of Early Earth and hypothetical extraterrestrial ecosystems. We studied the functionality and limits of key biogeochemical processes, such as photosynthesis, aerobic respiration, and sulfur cycling in salt crust-covered microbial mats from a tidal flat at the coast of Oman. We measured light, oxygen, and sulfide microprofiles as well as sulfate-reduction rates at salt saturation and in flood conditions and determined fine-scale stratification of pigments, biomass, and microbial taxa in the resident microbial community. The salt crust did not protect the mats against irradiation or evaporation. Although some oxygen production was measurable at salinity ≤ 30% (w/v) in situ , at saturation-level salinity (40%), oxygenic photosynthesis was completely inhibited and only resumed two days after reducing the pore water salinity to 12%. Aerobic respiration and active sulfur cycling occurred at low rates under salt saturation and increased strongly upon salinity reduction. Apart from high relative abundances of Chloroflexi, photoheterotrophic Alphaproteobacteria , Bacteroidetes , and Archaea, the mat contained a distinct layer harboring filamentous Cyanobacteria , which is unusual for such high salinities. Our results show that the diverse microbial community inhabiting this saltflat mat ultimately depends on periodic salt dilution to be self-sustaining and is rather adapted to merely survive salt saturation than to thrive under the salt crust. Importance Due to their abilities to survive intense radiation and low water availability hypersaline microbial mats are often suggested to be analogs of potential extraterrestrial life. However, even on Earth the limitations imposed on microbial processes by saturation-level salinity have rarely been studied in situ . While abundance and diversity of microbial life in salt-saturated environments is well documented, most of our knowledge on process limitations stems from culture-based studies, few in situ studies, and theoretical calculations. Especially oxygenic photosynthesis has barely been explored beyond 5M NaCl (28% w/v). By applying a variety of biogeochemical and molecular methods we show that despite abundance of photoautotrophic microorganisms, oxygenic photosynthesis is inhibited in salt-crust covered microbial mats at saturation salinities, while rates of other energy generation processes are decreased several fold. Hence, the complete element cycling required for self-sustaining microbial communities only occurs at lower salt concentrations.

Community homeostasis of coastal microbial mats from the Camargue during winter (cold) and summer (hot) seasons

“…Salinity may affect both photosynthesis and O 2 diffusion (Meier et al, 2021). Wieland and Kühl (2006) described that net photosynthesis versus irradiance in Camargue mats was almost unaffected by decreasing salinity (100‰–40‰), whereas increasing salinities (100‰–160‰) led to a decrease of net photosynthesis at each level of irradiance.…”

Divide and conquer: Spatial and temporal resource partitioning structures benthic cyanobacterial mats

“…Oxic to anoxic conditions vary across space and time and are a major factor in how nutrient cycling is partitioned spatially and temporally in BCMs, especially in layered mats. Links between these cycles are created through redox coupling, direct metabolic cooperation, and inhibition by or dependence on geochemical gradients (e.g., photosynthesis may be inhibited by high sulfide concentration; Meier et al, 2021). [Color figure can be viewed at wileyonlinelibrary.com] fully trace the diversity of carbon fixation and carbon cycling throughout BCM communities.…”

“…These gradients are driven by spatially variable sulfate reduction, sulfide oxidation, as well as transport via differential diffusion (Figure 3; Fike et al, 2008). Overlap between biogeochemical zones, such as sulfide and oxygen, can create microniches, allowing for distinct microbial specialization (Meier et al, 2021). Sulfide oxidation can occur within overlapping areas of light and sulfide concentrations or well below the photic zone by an entirely different set of specialized bacteria (Figure 3; Grünke et al, 2011;Jørgensen & Des Marais, 1986).…”

What Controls the Sulfur Isotope Fractionation during Dissimilatory Sulfate Reduction?

“…Dissimilatory sulfate reduction requires an electron donor, usually in the form of organic compounds, and in most marine habitats, sulfate respiration is primarily regulated by organic substrate supply rather than sulfate availability as sulfate concentrations in marine sediments are usually well above the half-saturation concentration for sulfate reduction. − The role of electron donors in sulfur isotope fractionation has been extensively studied with pure cultures of dissimilatory sulfate reducers, demonstrating that the limitation by electron donors or the presence of recalcitrant organic substrate increases the magnitude of isotopic fractionation. ,− Although there are some variations across species, sulfate reduction coupled to the oxidation of molecular hydrogen or simple organic acids such as lactate produced a relatively small isotope effect, while a larger sulfur isotope effect was obtained during the growth on carbohydrates or aromatic substrates (Figure ). With lactate as a sole electron donor, however, growth under lactate-limited conditions in a continuous culture increases the sulfur isotope discrimination between sulfate and sulfide up to over 50‰ (Figure ), highlighting that large isotope fractionation can occur even in the presence of labile substrates if they are present in a limited quantity.…”