Ecophisiology in Trichodesmium under global change

Trichodesmium’s dominant role in carbon and nitrogen cycling has prompted investigations examining the effects of rising sea surface temperatures and elevated atmospheric pCO2 (leading to ocean acidification) on the growth and abundance of this organism. We examined combined effects of elevated pCO2 , changes in light and nutrients on the physiology and gene expression of key genes in Trichodesmium. Genes that participate in nitrogen metabolism, Ci fixation, and photosynthesis were most affected by changes in pCO2, temperature and the time within the diurnal period. High pCO2 shifted transcript patterns of all genes, resulting in a more synchronized diel expression. Concurrently, we found no significant changes in the protein pools or in total cellular allocations of carbon and nitrogen (i.e. C : N ratio remained stable). Moreover, increased temperatures and high pCO2 resulted in higher C : P ratios. The plasticity in phosphorous stoichiometry combined with higher enzymatic efficiencies lead to higher growth rates. We demonstrate that shifted cellular resource and energy allocation among those components will enable Trichodesmium grown at elevated temperatures and pCO2 to extend its niche in the future ocean, through both tolerance of a broader temperature range and higher P plasticity.

Programmed cell death

(PCD) is an irreversible, genetically controlled form of cell suicide that is essential to promote and maintain genetic stability and is critical for the regulation of cellular and tissue homeostasis in metazoans. PCD has been observed in a variety of unicellular organisms including prokaryotic bloom-forming cyanobacteria, chlorophytes, dinoflagellates, diatoms, and coccolithophores. Trichodesmium also displays autocatalytic PCD in response to stressors such as oxidation, high irradiance, and Fe-depletion. In the oceans Trichodesmium forms extensive blooms in nutrient-poor tropical and subtropical regions. These massive blooms generally collapse several days after forming, but the cellular mechanism responsible along with the magnitude of associated C and N export, are as yet unknown. Our work from laboratory simulations demonstrate that extremely rapid development and abrupt, PCD-induced demise (within 2-3 d) of Trichodesmium blooms lead to greatly elevated excretions of transparent exopolymers and a massive downward pulse of particulate organic matter. Our results mechanistically link autocatalytic PCD and bloom collapse to quantitative C and N export fluxes and suggest that PCD may impact biological pump efficiency in the oceans.

Etai Landou, PhD student

The ocean is a significant sink of anthropogenic CO2, in large part because organic matter is exported to oceanic depths driving the biological sequestration of carbon in the ocean’s interior. Organic matter export depends on the supply of external nutrients to the euphotic zone (by processes such as deep mixing and biological fixation of atmospheric dinitrogen (N2)) and the subsequent production of organic matter by photosynthesis (defined as “new” production).

The Gulf of Aqaba offers a unique opportunity to observe, at high temporal resolution, both mechanisms supplying “new” nutrients. The oligotrophic Gulf is surrounded by land on three sides and characterized by a thermohaline circulation pattern caused by high evaporation rates, and exhibits strong seasonal variability mainly due to deep winter mixing and strong summer stratification.

My main goal is to understand the relative contribution of N2 fixation and deep winter mixing to “new” production and subsequent “export” in the northern Gulf of Aqaba and to simulate and predict the response of the system under changing environmental scenarios.


DEEPLEV deep mooring project

The Mediterranean Sea has nurtured and sustained its surrounding populations for thousands of years. Yet, food and energy requirements of increasing populations have contributed to a greater human (anthropogenic) footprint on the Mediterranean. The recent discoveries of large natural gas reservoirs (1.8% of world reserves) and possibly oil in the Levant Basin of the eastern Mediterranean Sea (EMS) have stirred excitement over the new prospects yet raise stakeholders concerns about the environmental risks involved in the large-scale exploitation of these offshore resources.
Marine hydrocarbon pollution affects pelagic, benthic, and coastal populations as well as commercially grown organisms. Primary producers and bacterioplankton form the basis of marine food webs and are essential for biogeochemical cycling of nutrients such as carbon (C), nitrogen (N), and phosphorus (P). Many studies have examined the response of individual species of algae or bacteria with several studies examining the integrated responses of natural communities of marine pelagic and coastal microbial populations including primary producers to either acute or chronic hydrocarbon pollution. Yet, the large variability of both pollutants and the natural environments/ecosystems make community responses hard to predict requiring experimentation according to specific locality and conditions.
This project will be funded starting October 2014, candidates for PhD are encouraged to apply.

Jerusalem Post Marine Station November 23, 2017


Nitrogen fixation

Photosynthesis and fixation of atmospheric dinitrogen which are two fundamental processes that are performed by organisms at the basis of aquatic food webs – the phytoplankton and bacterioplankton. Dinitrogen fixation is a biological transformation carried out only by a subgroup of prokaryotic organisms (diazotrophs) that can utilize atmospheric nitrogen (N2), unavailable for most organisms, and convert it into a form of nitrogen that is used for growth. This process is extremely important in many nitrogen-poor surface waters of the oceans, and injects a new source of bioavailable nitrogen to areas where nitrogen limits growth and primary production by the ocean’s tiny plants – the phytoplankton. In our research we explore how diazotrophs influence bio-geochemical cycling of carbon and nitrogen in the face of climatic changes. These changes include global warming and ocean acidification due to increased dissolution of atmospheric CO2 in the oceans.

Collaboration with Dr. Yeala Shaked (IUI- Hebrew University) on iron uptake of Red Sea populations of Trichodesmium (a globally important N2 fixer in the tropical and subtropical oceans with blooms extending over thousands of kilometers) has illustrated that the colonies actively take up and shuttle Fe along the filaments to the center of the colony where it is dissolved and assimilated into the cells. We have also demonstrated that the future projections of high CO2 in the oceans can enhance nitrogen fixation and growth of this marine cyanobacterium and indicate that Trichodesmium will thrive in the future warmer and more acidified oceans.

Close-up on dust-loaded puff, showing the entrainment of the dust within the colony core (Rubin et al., 2011, Nature geoscience)

Further research on other diazotrophs in the Gulf of Eilat shows that a large diversity including bacterioplankton. These are not restricted like the phytoplankton to the upper sunlit areas of the surface oceans, and can fix nitrogen in deep dark layers. We measure N2 fixation rates from oceanic zones that have traditionally been ignored as sources of biological N2 fixation; the dark, fully oxygenated, nitrate (NO3)-rich, waters of the oligotrophic Gulf of Aqaba and the eastern Mediterranean. Our results suggest that while N2 fixation may be limited in the surface waters of the oligotrophic Mediterranean and Red Seas, N2 fixation from the deeper and dark ocean layers may contribute significantly to new N inputs, yet these inputs are currently not included in regional or global N budgets.

Dina Spungin, PhD, Lab manager

PhD Title: Programmed cell death in cyanobacteria 

My research focuses on the factors which regulate programmed cell death (PCD) in cyanobacteria. Specifically, I study PCD in the marine cyanobacteria Trichodesmium which form extensive blooms in the tropical and subtropical surface-oceans. Trichodesmium undergoes an autocatalytic, genetically programmed cell death in response to environmental stressors such as high irradiance and Fe limitation. They have key enzymes of the eukaryotic PCD and several proteins from the metacaspase family. I study the role of PCD in blooms and cell death mechanism in Trichodesmium. My work involves both laboratory experiments with Trichodesmium cultures, and field experiments with natural Trichodesmium blooms. Molecular and physiological approaches are applied to examine expression of PCD in Trichodesmium at both the genetic and protein levels.


Trichodesmium bloom in the South West Pacific Ocean (New Caledonia). Photo by D. Spungin

Trichodesmium bloom in the South West Pacific Ocean (New Caledonia).
Photo by D. Spungin

Yael Tzubari, PhD student

PhD Title: Trichomes to blooms in the marine diazotrophic cyanobacterium – Trichodesmium

Trichodesmium is a filamentous, non-heterocystous cyanobacteria whose filaments (trichomes) are composed of 10-100s of cells with similar morphologies. Trichomes can be found as single filaments, spherical (“puffs”) or fusiform (“tufts”) colonies . The colonies provide unique habitats for other organisms (metazoans, bacteria, and viruses) and serve as hot-spots for microbial mediated nutrient transformations within the oligotrophic oceans. While this phenomenon is a well-known trait of Trichodesmium the mechanisms for the formation of these structures are not understood.

In my research, I am interested in determining what causes the single filaments to create colonies; to reveal the cues and mechanisms involved in creating colonies from single trichomes. My work will combine live-imaging microscopy as well as molecular and physiological techniques.




Biofilm prevention in the desalination industry

Limitations of global freshwater supplies have stimulated the application of desalination technology with desalinized water coming online worldwide at a rate of 40 to 50 million m3 d−1. Currently, about 50% of global desalination is based on filtration through reverse osmosis (RO) membranes requiring effective pretreatment procedures upstream to reduce fouling, maintain performance and extend membrane lifetime and to ensure the manufacturers requirements for membrane recovery yield. Transparent exopolymer particles (TEPs) are sticky, organic microgels, ranging in size from ∼0.4 to >200 μm, present in large numbers in all aquatic environments. Recently, TEPs have been implicated as an important factor in the development of aquatic biofilm and are part of the extracellular polymeric substances (EPSs) that form the matrix of microbial biofilms.
In our research we examined the direct involvement of these microgel particles in biofilm development. We showed that protobiofilm and TEPs in the feedwater contributed to fast development of biofilm and not EPSs generated by adhering, single bacteria, or bacterial aggregates. In addition, experiments comparing the initial stages of biofilm formation in filtered or in untreated seawater clearly illustrate the importance of protobiofilm and TEPs in accelerating aquatic biofilm formation.

Schematic illustration showing the involvement of organic polymers and colloids, TEP and protobiofilm in the initial stages of aquatic biofilm formation. Immediately upon exposure to seawater, organic polymers and colloids (a) and microgels such as uncolonized TEP (b) and protobiofilm (c) begin to attach to pristine surfaces. Single cells of planktonic bacteria also attach reversibly (d) or irreversibly (e) to conditioned surfaces. With time (minutes to hours) a contiguous coverage of mature biofilm (f) develops. From Bar-Zeev et al. 2013.PNAS

Desalination impacts on microbial coastal populations

The increasing importance and expansion of seawater desalination technologies and large scale coastal plants – enhances both the “visibility” and essentiality of ensuring environmental sustainability of the impacted coastlines. Our study (2015-2019) added important knowledge to the scant information that has been published either locally or globally to examine the impacts of desalination discharges on the coastal microbial communities comprising the foundation of the aquatic food webs. Our overarching goal in this project was to characterize and predict the responses of microbial and phytoplankton communities to their exposure to both enhanced salinities and chemical discharges resulting from desalination plants.

The comprehensive results of this study including the in-situ sampling, experimental manipulations, hydrodynamic simulations of plume and intake effects, and modeling brine (and temperature impacts) on the aquatic food-web all demonstrate the following. Impacts are influenced by both seasonality and site-specificity with salinity and temperature both driving biological changes. Therefore, site-specific monitoring and assessment of changes of the microbial populations is essential. Moreover, Coastal environments, exposed to long term discharge of brine, may exhibit cumulative chronic effects and affect the ecosystems more dramatically. The assessment of ecological impacts, from the rapidly expanding desalination industry, on coastal marine environments and their biota should be included as a routine monitoring tool and not be based solely on the results of short term studies such as this one.

Past Students

Past students and Post doctoral Fellows

Nurit Amitai, MsC 2018, Effects of Antiscalants from Seawater Desalinatio Discharges on Coastal Bacterial and Phytoplanktonic Communities of the Eastern Mediterranean Sea

Liel Magnezi, Msc 2018, Trichodesmium bloom formation

Dan Miller, PhD 2018, Assessing the physiological and compositional response of coastal microbial populations to increased pCO2 and to eutrophication

Natasha Belkin, PhD 2016, Impacts of seawater desalination discharges on coastal bacterial and phytoplanktonic communities

Reut Sorek Abramovich, PhD. Post-doc fellow, 2015 Toxins in Trichodesmium

Adi Levi, PhD 2015, Applying innovative nano-technology approaches to reduce biofilm development on membrane and surfaces in the desalination industry

Eyal Rahav, PhD 2013, Controls on dinitrogen fixation in the eastern                              Mediterranean

Edo Bar Zeev, PhD 2012, TEP and biofilm formation; MSc 2007, Nitrogen fixation in aquatic symbiotic associations

Itamar Avishai, MSc 2012, Programmed cell death in Trichodesmium

Sara Ohaion, MSc 2012, Molecular diagnostics of controls on N2 fixation

Ben Brinberg, MSc 2013, Microbial ecology of subterranean estuaries of                       Mediterranean coastline

Tali Yogev, PhD 2009, Nitrogen fixation in the eastern Mediterranean

Orly Levitan, PhD 2010, Impacts of CO2 on aquatic dinitrogen fixation; MSc 2005, Influence of CO2 on aquatic nitrogen fixation

Eric Ben David, Post-doc fellow 2010, Programmed cell death in Trichodesmium

Tamar Bsor-Rachamim, PhD 2010, Nutrient recycling by zooplankton in Lake Kinneret

Max Rubin, MSc 2009, Fe uptake in Trichodesmium

Sammy Frenk, MSc 2008, Ammonium supply for optimal growth of juvenile and mature thalli of Porphyra rosengurtii (Rhodophyta)

Gad Rosenberg, MSc 2007, Programmed cell death in Trichodesmium

Dovi Kelman, Post-doc fellow 2007, Natural products from Trichodesmium

Chen Sherman, MSc 2006, Effect of varying pH on Trichodesmium