Doctoral Programme on Marine Ecosystem Health and Conservation
 PhD Subject Catalogue Fifth Edition - 2014
Microbial diversity and its role in the resilience of large brown seaweeds
PhD Code: MARES_14_12:
  • Host institute 1: P3 - University of Bologna
  • Host institute 2: P1 - Ghent University
Research fields:
  • T1 - Future Oceans: temperature changes - hypoxia - acidifation
  • T2 - Understanding biodiversity effects on the functioning of marine ecosystems
  • Laura Airoldi
  • Olivier De Clerck
Contact Person and email: Laura Airoldi -

Subject description
Human activities are causing environmental and ecological changes of global significance. By a variety of direct and indirect mechanisms, anthropogenic pressures on ecosystems contribute to the loss of biodiversity, homogenization of biota and alteration of ecosystem processes, with profound consequences for ecosystem services and human economic and social activities (Airoldi et al 2008). Coastlines are no exception to this global trend. Coastlines harbor some of the most ecologically and socio-economically significant ecosystems on the planet (Harley et al. 2006). They play a crucial role in maintaining the health of the planet's ecosystems and serve as a valuable current and future food source for humankind. Ironically, the great wealth of coastal areas, whether in terms of fishing, tourism, international trade, or natural resources, makes the seeds of their own destruction. Europe, with 86 % of its coasts at either high or moderate risk (Airoldi & Beck 2007), ranks first of the regions whose coastal ecosystems are most threatened by degradation (Halpern et al. 2008). The consequences and costs of these changes must be fully understood and acknowledged.
Here we focus on microbial diversity, because the causes, patterns and consequences of changes in biodiversity at this level are still largely unexplored. Biofilms are highly complex communities in the natural, environment consisting of many hundreds of species. They are fundamental players in many ecosystem processes, including productivity and carbon and nitrogen turnover in food webs (Bengtsson et al. 2012), and influence the resilience and resistance of ecosystems to environmental change, by affecting the susceptibility of key-habitat forming species to diseases (Goecke et al. 2010). Much of the interactions of microbial communities, algae and ecosystem functioning are virtually unexplored.
Large, brown, canopy-forming seaweeds are foundation species that control structural complexity, productivity, nutrient cycling and high associated biodiversity in temperate rocky reefs (Steneck et al. 2002). They constitute an important source of substrata for microbial colonization (Michelou et al 2013). Their three-dimensional structure offers critical surface area in benthic marine habitats and provides temporary or permanent shelters and sediment traps. They provide a protected micro-niche for microbial colonisation and reproduction and release exudates that may serve as source of carbon for heterotrophic bacteria living on their surface (Armstrong et al. 2001, Goecke at al. 2010). In turn, bacteria can directly and indirectly affect the morphogenesis and growth of their host seaweeds (Hollants et al. 2013a). They produce plant growth-promoting substances, quorum sensing signalling molecules, and bioactive compounds that are responsible for normal development and growth of seaweeds. Also, bioactive molecules of associated bacteria determine the presence of other bacterial strains on seaweeds, and can protect the host from harmful entities present in the pelagic realm.
Canopy-forming algae are severely globally threatened. In Europe, and particularly in the Mediterranean Sea, conspicuous declines, sometimes to local extinction, have been reported in many regions, particularly in urban areas (Benedetti Cecchi et al 2001, Thibaud et al Airoldi and Beck, 2007, Mangialajio et al 2007, Perkol-Finkel & Airoldi 2010). These lost canopies are being replaced by species of lesser structural and ecological value such as turf-forming, ephemeral algae or sea urchin barrens (Airoldi 1998, Connell et al., 2014), causing a loss of important ecosystem services. The underlying causes of such a widespread loss are complex, involving interactions of multiple local anthropogenic and global climatic stressors (Perkol-Finkel & Airoldi 2010, Wahl et al., 2011, Strain et al., 2014). Several researchers have hypothesized that such widespread declines might be further accelerated by a growing impact of diseases on increasingly stressed and therefore chemically poorly defended seaweeds (Campbell et al 2011, Fernandes et al 2012). Recent meta-analyses completed within an ongoing MARES project have shown that nutrient enrichment interacts synergistically with a variety of other stressors, leading to amplified negative effects on canopy-forming algae (Strain et al., 2014). We also observed that management of nutrient enrichment would greatly increase the resilience of fucoid algae to climatic stressors, in particular to increasing temperature (Strain et al., in prep). The underlying mechanisms for such a negative synergistic effect are not clear, and we hypothesise these might be related to indirect effects on the microbial community. Indeed bacterial growth tends to be enhanced in eutrophic coastal marine systems, with potential direct and indirect feedbacks on the host species. Such effects could be particularly severe at elevated temperatures, as it has been shown that these can reduce the levels of chemical defences (furanones) in stressed thalli leading to colonization or proliferation by opportunistic pathogens (Fernandes et al. 2012).
Working with specimens of large brown seaweeds from the Mediterranean (namely retracting species of Cystoseira, Fucus virsoides), the candidate will address 3 key questions:
1) Describe the diversity of the microbial communities associated with model fucoid algae subject to different stress levels. We will first compare the microbiome diversity of model brown algae under a variety of environmental and human pressures. The sampling will be replicated at different locations and sites along the coasts of Italy, selected to cover a range of different levels of stressors (i.e. highly urbanised sites where severe canopy regression is in progress vs more pristine sites with dense stable stands of Cystoseira) and will be designed to: 1) identify the diversity of species associated; 2) their spatial and temporal scales of variation; and 3) the relationships with important environmental (e.g. hydrodynamics) and anthropogenic (e.g. nutrient concentration, sediment levels, or other pollutants) stressors that could affect the microbial community both directly or indirectly, by influencing the physiological status of the seaweeds. Bacterial diversity analyses will be carried out using 16S rRNA gene amplicon sequencing using NGS platforms, as described in Bengtsson et al. (2010). The healthy status of the seaweeds will be quantified by measuring parameters such as density of fronds, growth, productivity and photosynthetic efficiency (by using PAM fluorometry) and concentration of furanones, algal metabolites which are antagonistic of bacterial quorum sensing. The information will allow developing testable models relating the microbial diversity with environmental conditions and pressures, to be tested in subsequent experiments. Due to the seasonality of many of the target seaweeds (which have their growing season from spring to end of summer) the field sampling for these analyses will be done before the start of the PhD (by other members of Unibo research team) in order to allow the candidate student to be able to carry on the analyses already from the start of the PhD
2) Test hypotheses on microbial community assembly by comparing functional composition and phylogenetic diversity. The principles underlying the assemblage and structure of microbial communities are little understood and pose an issue of long-standing concern to the field of microbial ecology. Burke et al. (2011), studying microbial communities associated with Ulva, proposed a competitive lottery hypothesis which argues that ecological niches are colonized randomly from a pool of species with similar ecological function that can coexist in that niche. In the context of a bacterial community, this model implies that there are guilds of bacterial species, whose members are functionally equivalent with respect to their ability to colonize a particular niche (e.g., the surface of the seaweed), but that the composition of species is determined stochastically by recruitment from within those guilds. The results of Burke et al. (2011) are only partially in agreement with those of Hollants et al. (2013b) who reveals a strong impact of local environmental factors on the presence of some bacteria, while the presence of others reflects a predominant imprint of host evolutionary history. To address this question we will compare microbial diversity associated with Cystoseira compressa based on 16S rDNA signatures with a functional characterisation of the associated bacteria based using NGS technologies.
3) Explore experimentally the interactions between the alga and the microbial communities, and how these can be affected by changing environmental conditions and genetic background. Current knowledge suggests that seaweed–bacterial relationships depend on the capacity of seaweeds to produce organic matter (food) and oxygen which are utilized by bacteria (Goecke et al., 2010). Complementarily, associated bacteria provide CO2, minerals and PGRs which enhance growth and morphogenesis in seaweeds. Therefore both the genetic and physiological status of the seaweeds could affect seaweed biofilm-interactions, and in turn these could feed-back (either positively or negatively) on the thallus development or growth of the seaweeds. Based on the relationships identified in the first two steps of the project, we will design experiments manipulating critical environmental stressors (e.g. nutrient concentration) to establish a cause-effect relationship between relevant ecological stressors (either natural and/or anthropogenic) affecting the status of the seaweeds and the diversity of the associated communities. During these experiments we will also measure how these relationships in turn affect important properties of the system, such as productivity and persistence of the canopy forming seaweeds.
  • Airoldi, L. (1998) Roles of disturbance, sediment stress, and substratum retention on spatial dominance in algal turf. Ecology, 79, 2759-2770.
  • Airoldi, L., Balata, D. & Beck, M.W. (2008) The Gray Zone: Relationships between habitat loss and marine diversity and their applications in conservation. Journal of Experimental Marine Biology and Ecology, 366, 8-15.
  • Airoldi, L. & Beck, M.W. (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanography and Marine Biology: an Annual Review, 45, 345-405.
  • Armstrong E, Yan L, Boyd KG, Wright PG, Burges JG. (2001). The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461: 37-40.
  • Benedetti-Cecchi, L., Pannacciulli, F., Bulleri, F., Moschella, P.S., Airoldi, L., Relini, G. & Cinelli, F. (2001) Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Marine Ecology Progress Series, 214, 137-150.
  • Bengtsson, M.M., Sjotun, K. & Ovreas, L. (2010) Seasonal dynamics of bacterial biofilms on the kelp laminaria hyperborea. Aquatic Microbial Ecology, 60, 71-83
  • Bengtsson, M.M., Sjotun, K., Lanzén, A. & Øvreås, L. (2012) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp laminaria hyperborea. The ISME journal, 6, 2188-2198
  • Burke, C., Steinberg, P., Rusch, D., Kjelleberg, S. & Thomas, T. (2011) Bacterial community assembly based on functional genes rather than species. Proceedings of the National Academy of Sciences of the United States of America, 108, 14288-14293
  • Campbell AH, Harder T, Nielsen S, Kjelleberg S, Steinberg PD (2011) Climate change and disease: bleaching of a chemically defended seaweed. Global Change Biol 17: 2958–2970
  • Fernandes, N., Steinberg, P., Rusch, D., Kjelleberg, S. & Thomas, T. (2012) Community structure and functional gene profile of bacteria on healthy and diseased thalli of the red seaweed Delisea pulchra. Plos One, 7
  • Gianni, F., Bartolini, F., Airoldi, L., Ballesteros, E., Francour, P., Guidetti, P., Meinesz, A., Thibaut, T. & Mangialajo, L. (2013) Conservation and restoration of marine forests in the Mediterranean Sea and the potential role of Marine Protected Areas. Advances in Oceanography and Limnology, 4, 83–101.
  • Goecke, F., Labes, A., Wiese, J. & Imhoff, J.F. (2010) Chemical interactions between marine macroalgae and bacteria. Marine Ecology-Progress Series, 409, 267-299
  • Halpern, B. S., Walbridge, S., Selkoe, K. A., Kappel, C. V., Micheli, F., D'Agrosa, C. et al. 2008. A global map of human impact on marine ecosystems. Science, 319(5865), 948-952.
  • Harley, C.D.G., Hughes, A.R., Hultgren, K.M., Miner, B.G., Sorte, C.J.B., Thornber, C.S., Rodriguez, L.F., Tomanek, L. & Williams, S.L. (2006) The impacts of climate change in coastal marine systems. Ecology Letters, 9, 228-241
  • Hollants, J., Leliaert, F., De Clerck, O. & Willems, A. (2013) What we can learn from sushi: A review on seaweed–bacterial associations. FEMS Microbiology Ecology, 83, 1-16
  • Hollants, J., Leliaert, F., Verbruggen, H., Willems, A. & De Clerck, O. (2013) Permanent residents or temporary lodgers: Characterizing intracellular bacterial communities in the siphonous green alga bryopsis. Proceedings of the Royal Society B-Biological Sciences, 280, 1754
  • Joint I, Tait K & Wheeler G (2007) Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos Trans R Soc Lond B Biol Sci 362: 1223–1233.
  • Mangialajo, L., Chiantore, M. & Cattaneo-Vietti, R. (2008) Loss of fucoid algae along a gradient of urbanisation, and structure of benthic communities. Marine Ecology Progress Series, 358, 63-74.
  • Rao D, Webb JS & Kjelleberg S (2005) Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicate. Appl Environ Microbiol 71: 1729–1736.
  • Perkol-Finkel, S. & Airoldi, L. (2010) Loss and recovery potential of marine habitats: an experimental study of factors maintaning resilience in subtidal algal forests at the Adriatic sea. PLoS ONE, 5, e10791.
  • Schiel, D.R. & Foster, M.S. (2006) The population biology of large brown seaweeds: Ecological consequences of multiphase life histories in dynamic coastal environments. Annual Review of Ecology Evolution and Systematics, 37, 343-372.
  • Steneck, R.S., Graham, M.H., Bourque, B.J., Corbett, D., Erlandson, J.M., Estes, J.A. & Tegner, M.J. (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation, 29, 436-459.
  • Strain EM, Thompson,RJ, Micheli F, Mancuso FP, Airoldi L. 2014. Interactions of multiple stressors in driving the global loss of forests of canopy-forming algae to turf-forming algae and opportunities for remediation at local scale. Global Change Biology. In press
  • Thibaut, T., Pinedo, S., Torras, X. & Ballesteros, E. (2005) Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Alberes coast (France, North-western Mediterranean). Marine Pollution Bulletin, 50, 1472-1489.
  • Wahl M, Jormalaninen V, Eriksson BK, Dethier M, Karez R, Kruse I, Lenz M, Pearson G, Rhode S, Wikstrom SA, Olsen JL (2011) Stress ecology in Fucus: abiotic, biotic and genetic interactions. Advances in Marine Biology 59: 37-105

Expected outcomes
Each research question will form the basis of a chapter in the PhD thesis. The candidate will structure the thesis around at least 3 scientific papers (the individual chapters), with an introductory review section (with an aim for submission as a review paper) and a discussion section to give a coherent synthesis of the work outputs and suggestions for future work. The research is extremely novel and cutting-edge, and is aimed at understanding key ecological processes responsible for the structuring and persistence of valuable but threatened marine communities.  
The student will attend at least 2 leading international conferences over the course of the project, potentially including the Temperate Reef Symposium (Pisa, Italy 2016) and the 11th International Phycological conference (2017, location to be announced). 
The collaboration between UNIBO and UGent supervisors will enable the candidate to benefit from their extensive experience with experimental ecology (both in the field and the laboratory), algal biology and ecology, and microbial-algal interactions. We will also set up collaborations with chemists working at Unibo and Ughent, to quantify some of the most relevant molecules involved in the algal-microbial interactions (e.g. concentration of furanones).

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