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Marine Microbiology

Head of the group: Dr. Laura Steindler

Marine Microbiology research group (Established 2011)

Head of the group: Dr. Laura Steindler

Lab manager: Dr. Rinat Bar-Shalom

The Lab's research focuses on the following topics:

  • Host-microbe interactions (symbiosis in marine sponges)
  • Cell-cell signaling in host-associated microbiomes (quorum sensing)
  • Physiology and molecular biology of marine bacteria (e.g. SAR11) and their adaptations to the ultra-oligotrophic Eastern Mediterranean Sea
  • Photoheterotrophy in marine bacteria (proteorhodopsin, aerobic anoxygenic phototrophic bacteria)

Join us: We are recruiting M.Sc. and Ph.D. students. If you are interested please send your CV and research interests to: lsteindler@univ.haifa.ac.il

Our lab focuses on two main themes of marine microbiology. One relates to the adaptation of free-living heterotrophic bacteria to oligotrophic conditions, and the utilization of light energy to compensate for carbon starvation. The other focus is on adaptations of marine bacteria to life in symbiosis with invertebrate hosts, and more specifically with marine sponges.

Host-microbe interactions (symbiosis in marine sponges)

Today we look at animals as 'holobionts'. These comprise the eukaryotic host and microorganisms that are tightly associated to it. In fact it is now well accepted that animals exist only in partnership with symbionts that affect the health of such multi-organismal entities. Our laboratory investigates the interactions within holobionts using as model system marine sponges.

With sponges possibly being the earliest branching extant animal lineage, sponges are ideally evolutionary placed to inform our understanding of the early evolution of host-microbe symbioses.

We look at the molecular mechanisms involved in the establishment and maintenance of the interaction of the sponge with its microbial symbionts. One aspect is to determine how components of what could be considered an ancient innate immune system (of the sponge) may serve the sponge to differentiate between microbial symbionts and microbial food (or pathogens). Using substractive hybridization techniques we identified a sponge-gene containing a scavenger receptor cystein rich (SRCR) domain that was differentially expressed in the presence versus absence of cyanobacterial symbionts (Steindler et al, Mar Biotechnol 2007). Proteins featuring SRCR domains are either cell surface or secreted proteins and in vertebrates have functions related to host-defense during endocytosis. We hypothesized that sponge genes with SRCR domain that are differentially expressed in relation to presence/absence of microbial symbionts may have a function in the recognition of the symbiont.

Presently we are utilizing transcriptomic-based approaches to gain a more global overview of the genes that are differentially expressed in the sponge in function of the symbiotic state with cyanobacterial symbionts. Further, we seek for mechanisms of host-symbiont recognition also within the genomes of sponge symbionts. The latter are sequenced by next-generation sequencing, assembled by bioinformatic-binning methods, and then compared to available genomes of the phylogenetically clo sest free-living bacteria.

 

Quorum sensing in sponge holobionts

Quorum sensing (QS) is a system used by many bacteria to coordinate gene expression according to the density of their local population. It is based on the synthesis of signal molecules and on response regulator proteins that sense the concentration of the signal molecules and bind to gene-promoters to enhance or inhibit the expression of QS regulated genes. Pathogens use QS to coordinate the production of virulence factors, squid-symbionts use it to activate bioluminescence expression. Sponges harbor a remarkable diversity of microbial symbionts in an enclosed niche where signal molecules can accumulate and enable cell-cell interaction, such as QS. We have used community genome assembly and binning to investigate the uncultured majority of sponge symbionts and identify common N-acyl homoserine lactone QS systems (article in review). Our next conceptual step is to investigate the function(s) played by QS within sponge holobionts.

 

Sponges and biotechnology

 

Sponges are also a major reservoir of natural diversity, with an incredible range of different bacterial phyla that are potential source of new enzymes and small molecules of interest for the chemical industry and medicine. We use high-throughput microbial cultivation methods to try and cultivate such majority of yet-uncultured sponge symbionts. More specifically, we are adapting the successful 'dilution to extinction' technique, which has led to the cultivation of oligotrophic marine free-living bacteria such as the ubiquitous SAR11 clade, for the cultivation of sponge symbionts. Furthermore we use cosmid libraries, -omics techniques and bioinformatic analyses on DNA derived from the sponge microbiomes to search for genes responsible for the production of secondary metabolites of interest. In particular, we are interested in novel anti-microbials based on quorum-quenching mechanisms (inhibition of quorum sensing) in bacterial pathogens.

Photoheterotrophy in marine bacteria

Every drop of seawater contains about half a million bacteria, and the latter drive the cycles of energy and matter in the oceans. Despite their significance, our understanding of their physiology and their impact on marine energetic budgets is limited. Many marine heterotrophic bacteria are capable of light-mediated ATP production using proteorhodopsins (PR) proteins that, upon illumination, create a pH gradient across the cellular membrane. These organisms can therefore supplement energy obtained via consumption of exogenous carbon with PR derived ATP to meet their energetic requirements. While extensive work has examined the oceanic C cycle on the assumption that all energy must pass through photosynthetic primary production, by this mechanism solar energy can by-pass CO2 fixation. Yet few studies have tested the extent to which light-harvesting by PR can complement or substitute other energy source in pure cultures of marine bacteria, and little is known about the genetic mechanisms underlying the PR photoheterotrophic strategy. Even more limited is our understanding on the percent energetic contribution of PR directly in marine microbial consortia.

Our laboratory utilizes high-throughput microbial cultivation methods with oligtrophic seawater-based growth media and flow-cytometry to identify cells at very low cell densities (typical of those found in natural ecosystems) to isolate novel bacteria from the Eastern Mediterranean Sea. These bacterial cultures enable us to investigate the mechanisms of light-utilization in bacteria that are naturally abundant in the environment. Further we can obtain their genome sequences that serve not only to bring forward new hypotheses on cellular functions that can be tested using the microbial cultures, but also as reference genomes in environmental meta-omics studies run by our and other laboratories.

Further, we are developing physiologic methods to investigate the contribution (energetic/transport) of proteorhodopsin in natural marine microbial assemblages.

Publications

  • Saurav K, Teta R, Esposito G, Bar-Shalom R, Costantino V, Steindler L (2016) Isolation of marine Paracoccus sp. Ss63 from the sponge Sarcotragus sp. and characterization of its quorum-sensing chemical-signaling molecules by LC-MS/MS analysis. Israel Journal of Chemistry (in press)
  • Saurav K, Bar-Shalom R, Haber M, Burgsdorf I, Oliviero G, Costantino V, Morgenstern D, Steindler L (2016) In search of alternative antibiotic drugs: Quorum-quenching based anti-virulence potential in sponges and their bacterial isolates. Frontiers in Microbiology (in press)
  • Burgsdorf I, Slaby BM, Handley KM, Haber M, Blom J, Marshall CW, Gilbert JA,Hentschel, U, Steindler L (2015) Lifestyle evolution in cyanobacterial symbionts of sponges. MBio 6(3):e00391-15. Doi:10.1128/mBio.00391-15
  • Britstein M, Devescovi G, Handley KM, Malik A, Haber M, Saurav K, Teta R, Costantino V, Burgsdorf I, Gilbert JA, Sher N, Venturi V and Steindler L. (2016) A new N-acyl homoserine lactone synthase in an uncultured symbiont of the Red Sea sponge Theonella swinhoei. Applied and Environmental Microbiology 82(4):1274-1285
  • Zheng Q, Liu Y, Steindler L, Jiao N (2015) Pyrosequencing analysis of aerobic anoxygenic phototrophic bacterial community structure in the oligotrophic western Pacific Ocean. FEMS Microbiology Letters 362(8). Pii: fnv034. Doi: 10.1093/femsle/fnv034
  • Burgsdorf I, Erwin PM, López-Legentil S, Cerrano C, Haber M, Frenk S, Steindler L (2014)Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis. Frontiers in Microbiology 10;5:529, doi: 10.3389
  • Carini P, Steindler L, Beszteri S, Giovannoni SJ (2013) Nutrient requirements for growth of the extreme oligotroph 'Candidatus Pelagibacter ubique' HTCC1062 on a defined medium. The ISME Journal 7(3):592-602
  • Sun J, Steindler L, Thrash JC, Halsey KH, Smith DP, Carter AE, Landry ZC, Giovannoni SJ (2011) One Carbon metabolism in SAR11 pelagic marine bacteria. PLoS ONE 6(8):e23973
  • Steindler L, Schwalbach M, Smith DP, Chan F, Giovannoni SJ (2011) Energy starved Candidatus Pelagibacter ubique substitutes light-mediated ATP production for endogenous carbon respiration. PloS ONE 6(5):e19725

Laura Steindler

Education:

1998    BSc     Tel Aviv University

2000    MSc     Tel Aviv University

2005    PhD     Tel Aviv University

 

Post-doctoral training

2005-2008       ICGEB-Trieste, Italy                          Dr. Vittorio Venturi Lab

2008-2011       Oregon State University, OR, USA   Dr. Stephen Giovannoni Lab

 

Publications

  1. Saurav K, Teta R, Esposito G, Bar-Shalom R, Costantino V, Steindler L (2016) Isolation of marine Paracoccus sp. Ss63 from the sponge Sarcotragus sp. and characterization of its quorum-sensing chemical-signaling molecules by LC-MS/MS analysis. Israel Journal of Chemistry (in press)
  2. Saurav K, Bar-Shalom R, Haber M, Burgsdorf I, Oliviero G, Costantino V, Morgenstern D, Steindler L (2016) In search of alternative antibiotic drugs: Quorum-quenching based anti-virulence potential in sponges and their bacterial isolates. Frontiers in Microbiology (in press)
  3. Burgsdorf I, Slaby BM, Handley KM, Haber M, Blom J, Marshall CW, Gilbert JA, Hentschel, U, Steindler L (2015) Lifestyle evolution in cyanobacterial symbionts of sponges. MBio 6(3):e00391-15. Doi:10.1128/mBio.00391-15
  4. Britstein M, Devescovi G, Handley KM, Malik A, Haber M, Saurav K, Teta R, Costantino V, Burgsdorf I, Gilbert JA, Sher N, Venturi V and Steindler L. (2016) A new N-acyl homoserine lactone synthase in an uncultured symbiont of the Red Sea sponge Theonella swinhoei. Applied and Environmental Microbiology 82(4):1274-1285
  5. Zheng Q, Liu Y, Steindler L, Jiao N (2015) Pyrosequencing analysis of aerobic anoxygenic phototrophic bacterial community structure in the oligotrophic western Pacific Ocean. FEMS Microbiology Letters 362(8). Pii: fnv034. Doi: 10.1093/femsle/fnv034
  6. Burgsdorf I, Erwin PM, L?pez-Legentil S, Cerrano C, Haber M, Frenk S, Steindler L (2014) Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis. Frontiers in Microbiology 10;5:529, doi: 10.3389
  7. Carini P, Steindler L, Beszteri S, Giovannoni SJ (2013) Nutrient requirements for growth of the extreme oligotroph 'Candidatus Pelagibacter ubique' HTCC1062 on a defined medium. The ISME Journal 7(3):592-602
  8. Sun J, Steindler L, Thrash JC, Halsey KH, Smith DP, Carter AE, Landry ZC, Giovannoni SJ (2011) One Carbon metabolism in SAR11 pelagic marine bacteria. PLoS ONE 6(8):e23973
  9. Steindler L, Schwalbach M, Smith DP, Chan F, Giovannoni SJ (2011) Energy starved Candidatus Pelagibacter ubique substitutes light-mediated ATP production for endogenous carbon respiration. PloS ONE 6(5):e19725
  10. Smith DP, Kitner JB, Norbeck AD, Clauss TR, Lipton MS, Schwalbach MS, Steindler L, Nicora CD, Smith RD, Giovannoni SJ (2010) Transcriptional and translational regulatory responses to iron limitation in the globally distributed marine bacterium Candidatus Pelagibacter ubique. PLoS One 5:5:e10487
  11. Schwalbach M, Tripp HJ, Steindler L, Smith DP, Giovannoni SJ (2009) The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environmental Microbiology 12:490-500
  12. Licciardello G, Bertani I, Steindler L, Bella P, Venturi V, Catara V (2009) The Transcriptional activator rfiA is quorum-sensing regulated by cotranscription with the luxI homolog pcoI and is essential for plant virulence in Pseudomonas corrugata. Molecular Plant-Microbe Interactions 22:1514-1522
  13. Steindler L, Bertani I, De Sordi L, Schwager S, Eberl L, Venturi V (2009) LasI/R and RhlI/R quorum sensing in an environmental strain of Pseudomonas aeruginosa. Applied and Environmental Microbiology 75:5131-5140
  14. Netotea S, Bertani I, Steindler L, Venturi V, Pongor S (2009) A simple model for the early events of quorum sensing in Pseudomonas aeruginosa: modeling bacterial swarming as the movement of an activation zone. Biology Direct 12;4:6
  15. Steindler L, Bertani I, De Sordi L, Bigirimana J, Venturi V (2008) The presence, type and role of N-acyl homoserine lactone quorum sensing in fluorescent Pseudomonas originally isolated from rice rhizospheres is unpredictable. FEMS Microbiology Letters 288:102-111
  16. Steindler L, Devescovi G, Subramoni S, Venturi V (2008) A versatile plasmid biosensor useful to identify quorum sensing LuxR-family orphans in bacteria strains. Journal of Microbiological Methods 73:273-275
  17. Steindler L, Venturi V (2007) Detection of quorum sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiology Letters 266:1-9
  18. Steindler L, Schuster S, Ilan M, Avni A, Cerrano C, Beer S (2007) Differential gene expression in a marine sponge in relation to its symbiotic state. Marine Biotechnology 9:543-549
  19. Licciardello G, Bertani I, Steindler L, Bella P, Venturi V, Catara V (2007) Quorum sensing Pseudomonas corrugata and its involvement in plant pathogenesis. FEMS Microbiology Ecology 61:222-234
  20. Degrassi G, Devescovi G, Solis R, Steindler L, Venturi V (2007) Oryza sativa rice plants contain molecules which activate different quorum sensing N-acyl homoserine lactone biosensors and are sensitive to the specific AiiA lactonase. FEMS Microbiology Letters 269:213-220
  21. Pawlik JR, Steindler L, Henkel T, Beer S, Ilan M (2007) Chemical warfare on coral reefs: Sponge metabolites differentially affect coral symbiosis in situ. Limnology and Oceanography 52:907-911
  22. Oren M*, Steindler L*, Ilan M (2005) Transmission, plasticity and the molecular identification of cyanobacterial symbionts in the Red Sea sponge Diacarnus erythraenus. Marine Biology 148:35-41 [* equal contribution]
  23. Steindler L, Huchon D, Avni A, Ilan M (2005) 16S rRNA phylogeny of sponge-associated cyanobacteria. Applied and Environmental Microbiology 71:4127-4131
  24. Fine M, Steindler L, Loya Y (2004) Endolithic algae photoacclimate to increased irradiance during coral bleaching. Marine and Freshwater Research 55:115-121
  25. Steindler L, Beer S, Ilan M (2002) Photosymbiosis in intertidal and subtidal tropical sponges. Symbiosis 33:263-273
  26. Steindler L, Beer S, Peretzman-Shemer A, Nyberg C, Ilan M (2001) Photoadaptation of zooxanthellae in the sponge Cliona vastifica from the Red Sea as measured in situ. Marine Biology 138:511-515


Chapters in books:
Ferluga S, Steindler L, Venturi V (2008) N-acyl homoserine lactone quorum sensing in gram negative rhizobacteria. In: Secondary Metabolites in Soil Ecology. Vol 14. Karlovsky, P. (Ed), Heidelberg, Germany. Springer, pp. 69-92

 

ISF                              Photoheterotrophy: Physiological and genetic characterization of how dominant heterotrophic bacteria channel light energy into the ocean.

R&D Italy-Israel       A novel approach to fight antibiotic resistant pathogens: acquisition of quorum sensing inhibitors from marine sponges.

BSF                             Isolation of sponge-associated bacteria: a first step to reveal bacterial adaptations to life in symbiosis with a sponge.

Dr. Laura Steindler (Head of the Lab) laura3  
Dr. Rinat Bar Shalom (Lab manager) Rinat

Sponges harbor dense communities of diverse symbiotic microorganisms and there is increasing evidence that a majority of secondary metabolites found in the host extracts, originate from the symbiotic bacteria rather than by the host itself. Microbial symbionts utilize biosynthetic gene clusters for the production of secondary metabolites (e.g., PKS and NRPS). One of my goals is to determine what regulates the expression of these genes in situ within the sponge holobiont, in bacterial isolates from sponges and in heterologous systems. 

Dr. Markus Haber (post-doc) markus_picture2-1

My current research interests are in environmental microbiology, microbial ecology and physiology. I am working on two systems:

  • Host-microbe interactions – by comparative genomics I aim to find general and lineage specific adaptations to life of symbionts inside marine sponges.
  • Bacterial photoheterotrophy - Using diverse culture-dependent and –independent approaches my aim is to analyze the abundances, dynamics and functional roles of photoheterotrophy in the Eastern Mediterranean Sea.
Dr. Kumar Saurav (post-doc)  kumar_picture

Anti-virulence drugs are a new type of therapeutic agent aiming at virulence factors rather than killing the pathogen, thus providing less selective pressure for evolution of resistance. One promising example of this therapeutic concept targets bacterial quorum sensing (QS), because QS controls many virulence factors responsible for bacterial infections. The general aim of my project in the lab is to isolate and purify bioactive lead molecule that interfere with QS from sponge and its associated microorganisms.

Maya Britstein (PhD student)  maya_picture

The aim of my research is to understand molecular mechanisms underlying host-microbe interactions using the facultative association with the sponge Petrosia ficiformis with the endocellular photosynthetic Candidatus Synechococcus feldmannii, as a model system. 

Ilia Burgsdorf (PhD student)    ilia_picture

More than 25 phyla of bacteria compose the unique microbiome of one of the oldest metazoans on Earth, sponges.  Host-symbiont, symbiont-symbiont and phage-symbiont interactions within this complex holobiont (sponge-host and related microbes) are of great interest because of their long evolutionary history and genomic singularity. My study involves both bioinformatic (comparative genomics, metagenomic analyses) and molecular (genetic engineering) approaches. 

Matan Lahyani (MSc student)

matan_picture

Isolating and culturing novel oligotrophic bacteria from the Eastern Mediterranean Sea in view of further investigation that can provide a better understanding of element cycling in the marine ecosystem. Further I am interested in cellular mechanisms involved in starvation-survival in the wide-spread marine oligotroph Candidatus Pelagibacter ubique .

Sofia Sizikov (undergraduate student, .. and soon to be MSc student)

sofia_picture

Cyanobacterial symbionts of marine sponges have general adaptations to life inside the sponge. One of the suggested mechanisms of adaptation is the common absence of genes involved in synthesis of O-antigen in these symbionts (Burgsdorf et al., MBio 2015). In this project, I try to understand the role of O-antigen in cyanobacteria-sponge symbiosis by preventing its expression in free-living cyanobacteria.     

Nitzan Barak (undergraduate student)

nitzan_picture

Assessing the presence of PKS/NRPS genes, and testing the effect of biotic and abiotic conditions on PKS expression in isolated sponge symbionts.

 

Alumni

Dani Dubinski (MSc)            Thesis: Sub-mesoscale structuring of marine microbial communities.

Maya Britstein (MSc)            N-acyl homoserine lactone quorum sensing in the association between marine sponges and their symbiotic bacteria communities.

Ilia Burgsdorf (MSc)             Cyanobacteria from sponge holobionts: genomic adaptations and interactions with the microbiome.

Metagenomes of the microbiomes of Theonella swinhoei (Red Sea), Petrosia ficiformis Mediterranean Sea), Ircinia variabilis (Mediterranean Sea).

Draft genomes of sponge symbionts: Candidatus Synechococcus spongiarum

For information please contact us directly

If our topics are of interest to you, go ahead and contact us to apply for a M.Sc or Ph.D. position at our lab. We address our research questions by combining diverse methodologies, including molecular biology, physiology, imaging, chemistry, next generation sequencing and bioinformatics.

If you are interested please send your CV and a description of your interests to:

Email: lsteindler@univ.haifa.ac.il

Dr. Laura Steindler

Department of Marine Biology

Leon Charney School of Marine Sciences

University of Haifa,

Mt. Carmel, Haifa 3498838, Israel

Office: 972-4-8288987

Lab: 972-4-8280724

School Fax: 972-4-8288267

Field work

 

Dive sites

 

Sdot Yam - Israel

 

Achziv, Israel - EMP collection together with the Ilan-Lab

 

Adriatic Sea

 

Ligurian Sea – transplant experiments of P. ficiformis with Carlo Cerrano

 

Eilat