Dr. Tal Luzzatto Knaan is the head of the Functional Metabolomics lab. She earned her PhD in Biochemistry from the Hebrew University of Jerusalem. As a Vaadia-BARD postdoctoral fellow, she joined the lab of Prof. Pieter C. Dorrestein at the Skaggs School of Pharmacy and Pharmacological Sciences at the University of California, San Diego (UCSD). Her research focused on developing metabolomics-based approach to study microbial chemical communication, and exploring the marine chemical diversity for potential drug discovery. She did her second fellowship with Dr. Daniel Sher at the department of Marine Biology at the University of Haifa, studying the chemical interactions of marine picoplankton. In 2019, she started her own lab combining cutting-edge, multidisciplinary approach to explore the biological role, regulation, diversity and distribution of natural products in microbes and algae, and their potential biotechnological and medicinal applications. Tal is the head of the emerging Interdisciplinary Center for Metabolomics and Natural Products at the University of Haifa and active in the “Homeward Bound” Women in STEMM Leadership initiative.

Functional Metabolomics and Marine Natural Products

Natural products, are small molecules produced by an organism and have various biological roles in nature. Some serve as regulators of cellular processes, some as communication signals and some as defensive molecules that may be utilized in agriculture, biotechnology and medicine. Natural products have an incredibly long history. Traditionally, natural products from plants, animals and microorganisms were the source of virtually all medicinal treatments from folklore and tribal medicine to the era of antibiotics. The marine environment is highly prolific and treasure trove for novel chemistry for potential drug discovery that is largely understudied. We use functional metabolomics approach to explore the spatial and temporal patterns of small molecules to better understand their functional role in marine biological systems. This approach includes the characterization of the chemical space, the targeting of specific molecules to the biosynthesis and regulation.

Microbes
Microbes have an immense effect on the wellbeing of virtually all living organisms. Microbes are highly social and exist in complex communities with thousands of other organisms, where they engage in a myriad of interactions that are mediated by the exchange of molecules. The marine environment presents unexplored interaction and thus unexplored chemistry. Mining the chemistry in marine microbes is in the frontline of bioprospecting for the next generation of antibiotics. We apply mass spectrometry-based metabolomics, transcriptomics and genomics to correlate the chemotype to phenotype for the discovery of compounds and new biological functions.

Marine plants
Like land plants, marine plants are considered to be an overwhelming source of natural products, that act to protect and benefit the plant to thrive in its environment, however are less explored in that context. Marine plants such as algae (blue-green algae and seaweeds) seagrasses and mangrove plants also have an immense ecological role as primary producers in oceans, therefore understanding their metabolomic capacity is of great interest. The composition on natural products is very much dependent on the environmental conditions in a given niche. Hence, key questions we will be interested to ask are: What natural products are produced by the plant? When and where are they expressed? What are their biological/ecological roles? And how can we benefit from them?

Publications

1.    Luzzatto Knaan, T. (2022), Analytics for Grannies 001: Metabolomics. Analytical Science Advances. 
https://doi.org/10.1002/ansa.202200901

2.    Wu Z, Aharonovich D, Roth-Rosenberg D, Weissberg O, Luzzatto-Knaan T, Vogts A, Zoccarato L, Eigemann F, Grossart H-P, Voss M, Follows MJ, and Sher D. (2022) Single-cell measurements and modelling reveal substantial organic carbon acquisition by Prochlorococcus, Nature Microbiology.
https://doi.org/10.1038/s41564-022-01250-5

3.    Nahor O, Luzzatto-Knaan T#, Israel A#. (2022) A new genetic lineage of Asparagopsis taxiformis (Rhodophyta) in the Mediterranean Sea: as the DNA barcoding indicates a recent Lessepsian introduction. Frontiers in Marine Sciences. #Denote correspondence  https://doi.org/10.3389/fmars.2022.873817

4.    Fares Amer N and Luzzatto-Knaan T. (2022) Natural products of marine origin for the treatment of colorectal and pancreatic cancers: mechanisms and potential. International Journal of Molecular Sciences.
https://doi.org/10.3390/ijms23148048

5.    Librizzi V, Malacrinò A, Li Destri Nicosia MG, Barger N, Luzzatto-Knaan T, Pangallo S, Agosteo GE, Schena L. (2022) Extracts from Environmental Strains of Pseudomonas spp. Effectively Control Fungal Plant Diseases. Plants. 11(3):436. https://doi.org/10.3390/plants11030436

6.    Ding L, Bar-Shalom R, Aharonovich D, Kurisawa N, Patial G, Li S, He S, Yan X, Iwasaki A, Suenaga K, Zhu C, Luo H, Tian F, Fares F, Naman CB  Luzzatto-Knaan T. (2021) Metabolomic characterization of a cf. Neolyngbya cyanobacterium from the South China Sea reveals Wenchangamide A, a lipopeptide with in vitro apoptotic potential in colon cancer cells. Marine drugs 19(7): 397. https://doi.org/10.3390/md19070397

7.       Iwasaki A, Kurisawa N, Wang T, Li X, Luo H, Zhu C, Patial G, Yan X, He S, Luzzatto-Knaan T, Tian F, Naman CB, Suenaga K. (2021) Lingaoamide, a cyclic heptapeptide from a Chinese freshwater cyanobacterium Oscillatoria sp. Tetrahedron Letters. https://doi.org/10.1016/j.tetlet.2021.153214.

8.    Roth-Rosenberg D*, Aharonovich D*, Luzzatto-Knaan T*, Vogts A, Zoccarato L, Eigemann F, Nago N, Grossart HP, Voss M and Sher D. (2020) Prochlorococcus rely on microbial interactions rather than on chlorotic resting stages to survive long-term stress. mBio. *Denote equal contribution
https://mbio.asm.org/content/11/4/e01846-20

9.    Cao L, Gurevich A, Alexander KL, Naman CB, Leao T, Glukhov E, Luzzatto-Knaan T, Vargas F, Quinn R, Bouslimani A, Nothias LF, Singh NK, Sanders JG, Benitez RAS, Thompson LR, Hamid MN, Morton JT, Mikheenko A, Shlemov A, Korobeynikov A, Friedberg I, Knight R, Venkateswaran K, Gerwick WH, Gerwick L, Dorrestein PC, Pevzner PA and Mohimani H. (2019) MetaMiner: A scalable peptidogenomics approach for discovery of ribosomal peptide natural products with blind modifications from microbial communities, Cell Systems. https://doi.org/10.1016/j.cels.2019.09.004

10.    Melnik A, Vasquez-Baeza Y, Aksenov AA, Hyde E, McAvoy A, Wang M, Silva R, Protsyuk I, Wu J, Bouslimani A, Lim YW, Luzzatto-Knaan T, Comstock, W, Quinn RA, Wong R, Humphrey G, Ackermann G, Spivey T, Brouha SS, Bandeira N, Lin GY, Rohwer FL, Conrad DJ, Alexandrov T, Knight R, Dorrestein PC and Garg N. (2019) The molecular and microbial microenvironments in chronically diseased lungs associated with cystic fibrosis. mSystems
https://msystems.asm.org/content/4/5/e00375-19

11.   Luzzatto-Knaan T, Melnik AV and Dorrestein PC. Mass spectrometry uncovers the role of surfactin as an interspecies recruitment factor. (2019) ACS Chemical Biology 14: 459-467.
https://pubs.acs.org/doi/10.1021/acschembio.8b01120

12.   Bouslimani A, da Silva R, Kosciolek T, Janssen S, Amir A, Callewaert C, Dorrestein K, Zaramela L, Kim JN, Humphrey G, Schwartz T, Sanders K, Brennan C, Melnik AV, Luzzatto-Knaan T, Ackermann G, Zengler K, Knight R and Dorrestein PC. The impact of skin care products on skin chemistry and microbiome. (2019) BMC Biology 17 (1):47.
https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-019-0660-6

13.  Kapono CA, Morton JT, Bouslimani A, Melnik AV, Orlinsky K, Luzzatto-Knaan T, Garg N, Vázquez-Baeza Y, Protsyuk I, Janssen S, Zhu Q, Alexandrov T, Smarr L, Knight R and Dorrestein PC. (2018) Creating a 3D microbial and chemical snapshot of a human habitat. Scientific Reports. 8(1):3669.
https://www.nature.com/articles/s41598-018-21541-4

14.   Luzzatto-Knaan T, Garg N, Wang M, Glukhov E, Peng Y, Ackerman G, Amir A, Duggan BM, Ryazanov S, Gerwick L, Knight R, Alexandrov T, Bandeira N, Gerwick WH and Dorrestein PC. (2017) Digitizing mass spectrometry data to explore the chemical diversity and distribution of marine cyanobacteria and algae. eLife. https://doi.org/10.7554/eLife.24214.001

15.  Garg N, Luzzatto-Knaan T, Melnik AV, Caraballo-Rodríguez AM, Floros DJ, Petras D, Gregor R, Dorrestein PC, Phelan VV. (2016).  Natural products as mediators of disease. Natural Product Reports. 34:194-219.
https://doi.org/10.1039/C6NP00063K

16.  Garg N, Zeng Y, Melnik AV, Edlund A, Sanchez LM, Mohimani H, Gurevich A, Miao V, Schiffler S, Lim YW, Luzzatto-Knaan T, Cai S, Rohwer F, Pevzner PA, Cichewicz RH, Alexandrov T and Dorrestein PC. (2016) Molecular architecture of the microbial community of Peltigera lichen. mSystems. 1(6). pii: e00139-16.
https://doi.org/10.1128/mSystems.00139-16

17.  Petras D, Nothias LF, Quinn RA, Alexandrov T, Bandeira N, Bouslimani A, Castro-Falcón G, Chen L, Dang T, Floros DJ, Hook VY, Garg N, Hoffner N, Jiang Y, Kapono CA, Koester I, Knight R, Leber CA, Ling TJ, Luzzatto-Knaan T, McCall LI, McGrath AP, Meehan MJ, Merritt JK, Mills RH, Morton J, Podvin S, Protsyuk I, Purdy T, Satterfield K, Searles S, Shah S, Shires S, Steffen D, White M, Todoric J, Tuttle R, Wojnicz A, Sapp V, Vargas F, Yang J, Zhang C and Dorrestein PC. (2016) Mass spectrometry-based visualization of molecules associated with human habitats. Analytical Chemistry. 88:10775-10784.
https://doi.org/10.1021/acs.analchem.6b03456

18.  Wang M, Carver J, Phelan VV, Sanchez LM, Garg N, Peng Y, Watrous J, Nguyen D, Kapono CA, Luzzatto-Knaan T, Porto C, Bouslimani A, Melnik AV, Meehan MJ, Liu WT, Crusemann M, Boudreau PD, Esquenazi E, Sandoval-Calderon M, Kersten RD, Pace LA, Quinn RA, Duncan KR, Hsu CC, Floros DJ, Gavilan RG, Kleigrewe K, Northen T, Dutton RJ, Parrot D, Carlson EE, Aigle B, Michelsen CF, Jelsbak L, Sohlenkamp C, Pevzner P, Edlund A, McLean J, Piel J, Murphy BT, Gerwick L, Liaw CC, Yang YL, Humpf HU, Maansson M, Keyzers RA, Sims AC, Johnson AR, Sidebottom AM, Sedio BE, Klitgaard A, Larson CB, Boya PC, Torres-Mendoza D, Gonzalez DJ, Silva DB, Marques LM, Demarque DP, Pociute E, O’Neill EC, Briand E, Helfrich EJ, Granatosky EA, Glukhov E, Ryffel F, Houson H, Mohimani H, Kharbush JJ, Zeng Y, Vorholt JA, Kurita KL, Charusanti P, McPhail KL, Nielsen KF, Vuong L, Elfeki M, Traxler MF, Engene N, Koyama N, Vining OB, Baric R, Silva RR, Mascuch SJ, Tomasi S, Jenkins S, Macherla V, Hoffman T, Agarwal V, Williams PG, Dai J, Neupane R, Gurr J, Rodriguez AM, Lamsa A, Zhang C, Dorrestein K, Duggan BM, Almaliti J, Allard PM, Phapale P, Nothias LF, Alexandrov T, Litaudon M, Wolfender JL, Kyle JE, Metz TO, Peryea T, Nguyen DT, VanLeer D, Shinn P, Jadhav A, Muller R, Waters KM, Shi W, Liu X, Zhang L, Knight R, Jensen PR, Palsson BO, Pogliano K, Linington RG, Gutierrez M, Lopes NP, Gerwick WH, Moore BS, Dorrestein PC and Bandeira N. (2016) Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nature Biotechnology. 34:828–837.
https://doi.org/10.1038/nbt.3597

19.  Luzzatto-Knaan T, Melnik AV and Dorrestein PC. (2015) Mass spectrometry tools and workflows for revealing microbial chemistry. Analyst. 140:4949-4966.
https://doi.org/10.1039/C5AN00171D

20.  Luzzatto Knaan T, Kerem Z, Doron-Faigenboim A and Yedidia I. (2014) Priming of protein expression in the defense response of Zantedeschia aethiopica to Pectobacterium carotovorum. Molecular Plant Pathology.15:364-378.
https://doi.org/10.1111/mpp.12100

21.  Luzzatto Knaan T, Kerem Z, Lipsky A and Yedidia I. (2013) A systemic response of geophytes is demonstrated by patterns of protein expression and the accumulation of signal molecules in Zantedeschia aethiopica. Plant Physiology and Biochemistry. 71:218-225. 
https://doi.org/10.1016/j.plaphy.2013.07.014

22.  Tun OM, Lipsky A, Luzzatto Knaan T, Kerem Z and Yedidia I. (2012) The plant activator BTH promotes Ornithogalum dubium and O. thyrsoides differentiation and regeneration in vitro. Biologia Plantarum. 57:41-48.
https://doi.org/10.1007/s10535-012-0254-4

23.  Luzzatto Knaan T and Yedidia I. (2009) Induction of disease resistance in ornamental geophytes. Israel Journal of Plant Science. 57:401-410.
https://doi.org/10.1560/IJPS.57.4.401

24.  Golan A, Kerem Z, Tun OM, Luzzatto T, Lipsky A and Yedidia I. (2009) Combining flow cytometry and gfp reporter gene for quantitative evaluation of soft- rot bacteria in Ornithogalum dubium plantlets. Journal of Applied Microbiology. 108:1136-1144.
https://doi.org/10.1111/j.1365-2672.2009.04517.x

25.  Yishay M, Burdman S, Valverde A, Luzzatto T, Ophir R and Yedidia I. (2008) Differential pathogenicity and genetic diversity among Pectobacterium carotovorum subsp. carotovorum isolates from monocot and dicot hosts support early genomic divergence within this taxon. Environmental Microbiology. 10: 2746–2759.
https://doi.org/10.1111/j.1462-2920.2008.01694.x

26.  Luzzatto T, Golan A, Yishay M, Bilkis I and Yedidia I. (2007) Priming of antimicrobial phenolics during induced resistance response towards Pectobacterium carotovorum in the ornamental monocot calla lily. Journal of Agricultural and Food Chemistry. 55: 10315-10322.
https://doi.org/10.1021/jf072037+

27.  Luzzatto T, Yishay M, Lipsky A, Ion A, Belausov E and Yedidia I. (2007) Efficient, long-lasting resistance against the soft rot bacterium Pectobacterium carotovorum in calla lily provided by the plant activator methyl jasmonate. Plant Pathology. 56: 692-701.
Cover page: Plant Pathology. (2007) 56: August issue.
https://doi.org/10.1111/j.1365-3059.2007.01622.x

28.  Nerya O, Ben-Arie R, Luzzatto T, Musa R, Khativ S and Vaya J. (2006) Prevention of Agaricus bisporus postharvest browning with tyrosinase inhibitors. Postharvest Biology and Technology. 39:272–277.
https://doi.org/10.1016/j.postharvbio.2005.11.001

The Rilov Lab is based at the Israel Oceanographic & Limnological Research Institute (IOLR) on the coast of Haifa. Our lab studies diverse aspects of marine community ecology and conservation. The focal study systems are coastal benthic communities, mostly rocky shores and subtidal rocky reefs, but we are also involved in research on other systems and organisms.
 
We study the patterns and dynamics of community structure and biodiversity on rocky reefs, and the processes that shape them, including recruitment, species interactions, bioinvasions and climate change. We also investigate the impacts of overfishing (and, conversely, marine reserves) on benthic communities, and attempt to assess the ecosystem functions and services that marine systems provide along the Israeli Mediterranean and Red Sea shores.

We do our investigations by a combination of field surveys and monitoring, and field and lab experiments. In the past few years we have constructed several innovative experimental facilities to test the impacts of climate change (ocean warming and acidification) and bioinvasions on both species and communities. Our research includes several international collaborations (e.g., with the USA and Germany).

For more details visit the Lab website: www.rilovlab.com

Daniel Sher is a Professor of Marine Biology at the Leon H. Charney School of Marine Sciences, University of Haifa (Israel).  Daniel completed his undergraduate and PhD studies at the Hebrew University of Jerusalem, followed by postdoctoral studies at MIT.  His main research interest lies in Aquatic Chemical Ecology and Microbial Oceanography – understanding the way aquatic organisms communicate through chemistry, the chemicals that mediate these interactions, and the way these interactions and chemicals affect entire ecosystems. Most of the people in his lab currently study how Prochlorococcus, a tiny marine cyanobacterium and the most abundant photosynthetic organism on Earth, interacts with co-occurring marine bacteria. Other projects in the lab focus on understanding the causes for jellyfish blooms (including whether their associated bacteria are involved in bloom growth and decline), and on developing methods to use natural marine bacterial communities as biosensors for pollution. Daniel is also a member of the steering committee of the University of Haifa Data Science Research Center, and of the outreach committee of the School of Marine Sciences. He is married, has three kids and a dog, and in his spare time loves hiking, cooking and photography.

Our lab studies marine chemical ecology – the way aquatic organisms communicate through chemistry, the chemicals that mediate these interactions, and the way these interactions and chemicals affect entire ecosystems. This is a fascinating field of research that combines ecology, limnology/oceanography, biochemistry, molecular and cellular biology, physics and computational biology. In addition, studying these interactions often brings with it the discovery of novel chemical compounds which have biotechnological, pharmacological or medical uses – antibiotics, for example, are often synthesized by microorganisms in order to fight other microbes. Some of the questions we are interested in are: Do marine bacteria communicate using chemical signals? What are the roles of toxins in jellyfish, sea anemones, coral and hydra? How do marine invertebrates protect themselves against pathogens? Can understanding such interactions help us model marine communities and predict how they will change in a changing world?

2010-                Lecturer, Department of Marine Biology, Charney School of Marine Sciences, Haifa University, Israel

2007-2010      Post-doctoral Fellow, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, USA.

2000- 2008   PhD Summa cum Laude, Hebrew University, Jerusalem, Israel. Mentor: Prof. Eliahu Zlotkin,
                            Thesis Title: Biological Role of a Non-Nematocystic Toxin in Cnidaria – An Exercise in Chemical Ecology.

1997 – 2000    B.Sc. magna cum laude in Biology, the Hebrew University of

Prof. Smadar Ben-Tabou de-Leon obtained her PhD degree at the Racah Institute of Physics, at the Hebrew University in Jerusalem, on the optical properties of thin layers of semiconductors. She then did a first post-doctorate fellowship on the use of porous silicon surfaces for the detection of neural activity, under the supervision of Prof. Amir Sa’ar at the Hebrew University. In her second post-doctorate at the lab of Prof. Eric Davidson at Caltech, she made the transition to developmental and evolutionary biology and investigated the regulatory networks that drive the development of the sea urchin embryo. In 2012 she started her own laboratory at the University of Haifa, where she studies the biological regulation of biomineralization in the sea urchin larva. Her lab discovered that the molecular control of the sea urchin larval skeleton is similar to the regulation of blood vessel formations in vertebrates and humans. This illuminates how biomineralization evolved rapidly by co-opting ancestral developmental programs for organic scaffolds. Prof. Ben-Tabou de-Leon is currently the head of the Department of Marine Biology at the Charney school of Marine Sciences. She has published more than 30 peer-reviewed papers in theoretical and applied physics and biological sciences. Her work significantly contributed to the understanding of the genetic and cellular regulation of developmental processes and to the evolution of biomineralization. She is an associate editor of Frontiers in Ecology and Evolution and Frontiers in Cell and Developmental Biology. She is married, has four kids, two cats and on her spare time she likes playing pokemon-go, jogging and hiking.

Networks of regulatory genes control the differential expression of regulatory and structural genes and by that initiate and control the development of the body plan. Evolutionary changes of the functional organization of developmental gene regulatory networks are therefore the key molecular mechanism underlying evolutionary change of animal morphology. However, the relation between gene regulatory networks and the developmental tasks they execute is not always apparent: How do gene regulatory networks control complex developmental processes? How do changes in the regulatory circuitry translate into morphological changes and how do they lead to evolutionary innovations in the body plan? These questions lay at the most fundamental level of our understanding of developmental processes and their evolution. I address these questions by studying regulatory circuits that control specification, differentiation and morphogenesis in the sea urchin embryo and comparing them to regulatory circuits that control similar processes in in other organisms. In my work I combine novel high-through put experimental techniques with mathematical modeling, to further our understanding of the dynamic molecular control of developmental processes and their evolution.

Read more on the Gene Regulation in Development and Evolution laboratory webpage.

Professor Laura Steindler obtained her PhD degree from Tel Aviv University, Israel, on the topic of sponge-bacteria interactions. She then did a first post-doctoral fellowship on rhizosphere bacteria and the involvement of quorum sensing gene-regulation in plant-microbe interactions, in the laboratory of Dr. Venturi at ICGEB, Trieste. In her second post-doctorate, at the laboratory of Dr. Giovannoni (OSU, Oregon, USA) she worked on the marine SAR11 clade, which is the dominant marine bacterium, worldwide, and she deciphered, for the first time, the function of proteorhodopsin in these ecologically important microorganisms. In 2011 she started her own laboratory at University of Haifa, Israel, where she continues studying both sponge-microbe interactions as well as genomic adaptations of bacteria to nutrient deplete oceanic regions. Dr. Steindler is on the Editorial Board of Applied and Environmental Microbiology, and associate Editor in Frontiers in Microbiology. She is author of more than 40 peer-reviewed publications. Dr. Steindler has widely advanced the field of microbial sponge symbiosis and is considered an expert on symbiont genomics and transcriptomics, where she applies cutting-edge next-generation sequencing approaches and advanced bioinformatics.

My laboratory is interested in two major research areas:
1) proteorhodopsin phototrophy including adaptations to starvation in marine heterotrophic bacteria, and
2) sponge-microbe interactions, and the isolation of sponge-bacterial-symbionts using high-throughput dilution to extinction techniques.

1. PROTEORHODOPSIN PHOTOTROPHY

It is well known that phytoplankton can convert light energy into chemical energy, but the discovery of proteorhodopsins acting as light-powered proton pumps in heterotrophs is only a decade old. In a recent study I began unraveling the role of this protein in Candidatus Pelagibacter ubique, a dominant marine bacterium in the ocean’s photic zone. In this bacterium respiration of exogenous carbon is reduced in the light probably as a result of proteorhodopsin-mediated ATP production. Our lab is interested in focusing on the many unanswered questions in this system. Specifically, we will be: i) investigating the genetic mechanisms underlying physiological responses to light, ii) understanding when these light mediated energy harvesting mechanisms are utilized in nature, iii) establishing how similar or different are the mechanisms of utilization of PR mediated ATP production in a variety of important marine bacteria that can be cultured in the laboratory.

2. SPONGE-MICROBE INTERACTIONS

Another topic of research that drives the research in our lab is the symbiotic interactions between bacteria and marine invertebrates, with emphasis on sponges.

Sponges harbor specific bacterial communities (heterotrophic and autotrophic) that differ from those present in the surrounding water. These bacterial symbionts are of high interest not only for their important ecological role in marine symbiotic ecosystems, but also because they produce a wide range of secondary metabolites that can be used for the development of new pharmaceuticals. Most of these bacteria have not been isolated in culture. One focus of my lab is to develop methods to culture such previously uncultured organisms and characterize their physiology and chemistry. Another theme we address is the study of signals that maintain sponge-bacteria symbioses which leads to the question of how a sponge differentiates between symbiotic bacteria and bacteria that can be phagocytozed as food.