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Microbial BIOdiversity – CLIMAte feedbacks during environmental crises in semi-enclosed basins: lessons from the Late Miocene (Messinian)

Periodic Reporting for period 1 - BIOCLIMA (Microbial BIOdiversity – CLIMAte feedbacks during environmental crises in semi-enclosed basins: lessons from the Late Miocene (Messinian))

Reporting period: 2016-01-01 to 2017-12-31

BIOCLIMA focused on the impact of climate change on the microbial biodiversity in semi-enclosed basins. In particular, the project looked into ecosystem response to environmental crisis during the late Miocene (Messinian) salinity crisis (MSC) in the Mediterranean Sea. In the light of the scarcity to absence of body fossils in the Messinian sedimentary sequences, BIOCLIMA used a multidisciplinary approach, combining inorganic and organic geochemical proxies, for paleoclimate, paleoenvironmental and paleoecological reconstructions.

The project aimed to analyze the Messinian sediments for climate variations across the pronounced environmental change that affected the Mediterranean Sea during the Late Miocene. The ultimate goal was to investigate the response of marine microorganisms to the above mentioned changes at the onset of the MSC.
The first phase of the work (WP1) studied the Messinian strata deposited in three key areas of the Mediterranean Basin: 1) the Piedmont Basin (NW Italy), 2) the Sorbas Basin (SW Spain) and 3) the Caltanissetta Basin (Sicily, Italy). The Piedmont Basin was selected for the pilot study. Four main types of deposit with a characteristic cyclical pattern were studied: shales (organic-rich, also called “sapropels”), marls, carbonates and gypsum (Fig. 1). Sedimentological, geochemical (chemical elements) and geomicrobiological (molecular fossils) data allowed to demonstrate the mutual dependence between sedimentary cyclicity and astronomical climate oscillations, showing that during more humid phases freshwater discharge into the basins increased and controlled the deposition of organic-rich layers. Our dataset also provides evidence of wind-dominated, more arid phases during the deposition of marls and gypsum.

During the second phase of the work (WP2), mineralogical and petrographic observations, isotopic (carbon and oxygen) and especially geomicrobiological (molecular fossils) analyses aimed to assess the chemical and physical parameters of the Messinian waters. The main results obtained are:
1) Traces of extreme conditions. Molecular fossils sourced by extremophilic archaea (i.e. halophiles) archived in the MSC sediments suggest an increase of salinity. At the same time, other archaeal molecules point to the existence of persistent marine conditions in the upper water column. We speculate that the observed archaeal assemblage do not necessarily account for basin-wide seawater evaporation, but may reflect stratification and hypoxia like in some modern stratified basins (e.g. the Black Sea).
2) Primary production and stratification. Terrestrial molecular fossils indicate the intensification of terrigenous organic matter input during the deposition of shales (humid phases), driven by enhanced riverine runoff. Coeval increases in barium content, a common paleoproductivity proxy, agree with an enhanced nutrient supply during humid periods, promoting phases of eutrophication in the basin (Fig. 2). A concomitant effect was the intensification of water column stratification and the establishment of reducing bottom conditions, which were most likely responsible for the decline of eukaryotes.
3) Carbon cycle perturbation. The BIOCLIMA project used a Mediterranean marginal basin as natural laboratory for monitoring carbon cycling during the MSC. Carbon isotopes from different sources (carbonate minerals, calcareous microfossils, and molecular fossils) revealed a strong shift at the onset of the crisis, confirming a significant perturbation of the carbon cycle.
4) Variation of seawater temperatures. BIOCLIMA provided for the first time estimates for Messinian Mediterranean surface seawater temperature (SST), using independent paleotemperature proxy based on archaea molecules. Interestingly, the SST reconstructed for the initial phase of the crisis in the northern Mediterranean are surprisingly similar to modern average northern Mediterranean SSTs (~ 18°C).

In the third phase (WP3), the project investigated the impact of the MSC on the marine microbial community. In particular, the geomicrobiological data revealed the presence of microorganisms able to take advantage from the changing environment at the onset of MSC. For instance, ubiquitous filamentous fossils interpreted as remains of sulfide-oxidizing bacteria were recognized in all studied lithologies, representing a common, but poorly constrained biological component of the MSC (Fig. 1D). A diversification of archaeal molecular fossils is also documented at the onset of the MSC: planktic marine archaea survived the advent of the crisis but, at the same time, new archaeal organisms typical of more extreme conditions appeared (Fig. 2).

Dissemination activities:
- 1 manuscript published in Organic Geochemistry
- 1 manuscript submitted for publication to Marine Geology
- 3 manuscrip
The BIOCLIMA project has achieved the following breakthroughs:
a) Climate. BIOCLIMA has reconstructed the high frequency (20 myr) climatic fluctuations during the MSC. This study revealed that no major climate change occurred at the onset of the MSC.
b) Environmental parameters. BIOCLIMA has identified the predominant climate (humidity vs aridity) and environmental (salinity, oxygenation, temperature and fertilization of seawater) parameters, which characterized the advent of the MSC and dramatically influenced biological communities.
c) Microbes. BIOCLIMA provides a first complete molecular fossils inventory for the MSC; compounds from the domains Archaea, Bacteria and Eukarya were identified.
d) Carbon cycle. The high amount of organic matter found in the Messinian sediments indicates their potential to store organic carbon, agreeing with peculiar conditions at the seafloor that favored organic carbon preservation. This new approach fosters the idea of a deep, strongly stratified sea instead of a “normal” shallow water, hypersaline basin.

The obtained results have also impacts of interest for a broader audience.
Economic impacts: a) The high contents of organic matter found in the MSC deposits indicates that they are potential source rocks for both liquid and gaseous hydrocarbons. b) This study provides a complete overview of the chemical elements stored in the Messinian sediments, some of which are of economic value (e.g. zirconium, titanium, potassium, sulfur) and their future potential exploitation will benefit from the study on how climatic controlled the sediment chemistry.
Search for extraterrestrial life. The inventory of microbial communities preserved within evaporitic deposits may help to identify potential molecular signatures of past or present life in planets like Mars, where extensive sulfate minerals have been documented.
Link with other EU-projects. The study of Messinian microbial life and its metabolic activity perfectly complements the EU-funded COST action “MEDSALT” and Marie Curie ETN “SALTGIANT”, both aiming to create a scientific network to study the largest and most recent “salt giant” on Earth: the Messinian evaporites.
Schematic reconstruction of the water column structure during the early phases of the MSC
Outcrop pictures of the Pollenzo section (Piedmont, Italy; from Natalicchio et al., 2017)