Short communicationInfluence of bacteria on the response of microalgae to contaminant mixtures
Introduction
Microalgae as primary oxygen producers in aquatic ecosystems are of prime ecological importance, and represent the first trophic level in the aquatic food web (Azam and Malfatti, 2007, Field et al., 1998). The region surrounding individual algal cells, named the phycosphere, enriched in exuded organic molecules, is considered as an aquatic analogue of the rhizosphere where microorganisms interact with plants in the terrestrial ecosystem (Seymour et al., 2017). Within the phycosphere, microalgae interact with bacteria within a large range from symbiosis to parasitism, conferring advantages or disadvantages to both partners (Bell and Mitchell, 1972). The mechanisms of interactions between bacteria and phytoplankton are diverse and involve specific cellular processes and fine communication (e.g. quorum sensing) (Amin et al., 2012). Such mechanisms may result in antibacterial or algaecide activities (Mu et al., 2007, Ribalet et al., 2008) or substrate competition as experimentally observed between manipulated consortium of microalgae and bacteria (Le Chevanton et al., 2013). On the other hand, the presence of bacteria could offer to microalgae a capacity for tolerance and adaptation to stressful conditions, such as chemical exposure. Indeed, the heterotrophic metabolism of highly diverse bacterial communities in the field and their ability to degrade, metabolize and immobilize a large number of organic and inorganic compounds (Bouwer and Zehnder, 1993, Bruins et al., 2000), make it possible to assign them an ecological role of protecting microalgae, particularly in polluted environments. It can also be hypothesized that microalgal growth may be further improved when the latter are associated with bacteria subjected to chronic contaminants that could develop greater tolerance capacities than naive bacteria and therefore allow microalgae to benefit from these bacterial capacities to cope with pollutants (Bauer et al., 2010).
Therefore, the main hypothesis tested in this study proposes that the presence of bacteria with degrading or immobilizing ability would reduce the sensitivity of microalgae to organic or metal contaminants, counterbalancing any potential bacterial algaecide activity.
In order to test this hypothesis, the present study focused on the effect of a sediment elutriate issued from the resuspension of polluted sediments on the growth of two microalgae strains commonly found in marine environments: Isochrysis galbana, a small prymnesiophyte, and Thalassiosira delicatula, a centric diatom. Isochrysis galbana is a well-known phytoplankton species, traditionally used in aquaculture and biotechnology due its capacity to produce large biomass (Williams and Laurens, 2010) whereas Thalassiosira delicatula represents a model for diatom study, belonging to a genus widely distributed throughout the world’s oceans (Armbrust et al., 2004). Both strains were growing either in axenic or non-axenic condition, i.e. associated with bacteria naturally selected during culture selection and maintenance processes. The growth of xenic and axenic strains were compared when exposed to the total (including native bacteria) or dissolved fraction of the resuspended sediment, or artificial mixtures containing either the main metallic or organic contaminants found in these sediments.
Section snippets
Elutriate and filtered elutriate preparation
The elutriate was obtained by mixing seawater (3/4 by volume) and sediment (1/4) sampled in February 2015 from the Bizerte Lagoon, for 12 h, followed by decantation for 12 h. The elutriate thus represented the supernatant obtained after decantation. It still contained unsettled particulate matter, resident bacteria and water-soluble contaminants. The filtered elutriate was obtained after filtration of the elutriate on a 0.2 μm membrane, leading to a sterile mixture with only the dissolved
Differential sensitivity of axenic microalgal strains to contaminants
Axenization of both algal strains was successfully maintained during the present study, as no bacterial cells were observed using epifluorescence microscope and culture techniques performed just before the experiments. A significant reduction in the growth rates of both axenic strains was observed when supplemented with the total elutriate, but not with the filtered elutriate (Fig. 1A). A reduction of light availability due to the presence of large particles in the total elutriate is unlikely
Acknowledgments
We would like to thank the two reviewers for their constructive comments. This study was supported by the RISCO and PHYCOVER projects, which were funded by the French National Agency for Research (respectively, ANR-13-CESA-0001 and ANR-14-CE04-0011). We should like to thank Chrystelle Bancon-Montigny (UMR 5559 HydroSciences Montpellier) and Catherine Gonzalez (Ecole des Mines d’Alès, Alès), for providing the analyses and the artificial mixtures of pesticides and metals used in this study.
References (32)
- et al.
Impact of contaminated sediment elutriate on coastal phytoplankton community (Thau lagoon, Mediterranean Sea, France)
J. Exp. Mar. Biol. Ecol.
(2017) - et al.
Bioremediation of organic compounds — putting microbial metabolism to work
Trends Biotechnol.
(1993) - et al.
Microbial resistance to metals in the environment
Ecotoxicol. Environ. Saf.
(2000) - et al.
Degradation of chloroacetanilide herbicides and bacterial community composition in lab-scale wetlands
Sci. Total Environ.
(2015) - et al.
Coupling algal biomass production and anaerobic digestion: production assessment of some native temperate and tropical microalgae
Biomass Bioenergy
(2014) - et al.
Screening and selection of growth-promoting bacteria for Dunaliella cultures
Algal Res.
(2013) - et al.
Enhanced degradation of prometryn and other s-triazine herbicides in pure cultures and wastewater by polyvinyl alcohol-sodium alginate immobilized Leucobacter sp. JW-1
Sci. Total Environ.
(2018) - et al.
Isolation and algae-lysing characteristics of the algicidal bacterium B5
J. Environ. Sci.
(2007) - et al.
Consequences of contaminant mixture on the dynamics and functional diversity of bacterioplankton in a southwestern Mediterranean coastal ecosystem
Chemosphere
(2016) - et al.
Differential effect of three polyunsaturated aldehydes on marine bacterial isolates
Aquat. Toxicol.
(2008)
Biological and chemical transformation of atrazine in coastal aquatic sediments
Chemosphere
Bioremediation of diuron contaminated soils by a novel degrading microbial consortium
J. Environ. Manag.
Interactions between diatoms and bacteria
Microbiol. Mol. Biol. Rev.
The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism
Science
Microbial structuring of marine ecosystems
Nat. Rev. Microbiol.
Effects of bacterial communities on the sensitivity of the phytoplankton Stephanodiscus minutulus and Desmodesmus armatus to tannic acid
Aquat. Microb. Ecol.
Cited by (25)
Application of confocal microscopy and flow cytometry to identify physiological responses of Prorocentrum micans to the herbicide glyphosate
2024, Marine Environmental ResearchEffects of polycyclic aromatic hydrocarbons on marine and freshwater microalgae – A review
2023, Journal of Hazardous MaterialsValorization of swine wastewater in a circular economy approach: Effects of hydraulic retention time on microalgae cultivation
2021, Science of the Total EnvironmentCitation Excerpt :This behavior is evidenced by the decrease in DO concentration in this period, which can be a reflection of the consumption of this variable by bacteria (Fig. S1), also chl-a concentration decay during the first week of operation. In the initial operation weeks, it is common in any reactor constituted by the bacteria and microalgae consortium that the bacterial activity exceeds that of the photosynthesizing organisms, reinforcing that for the microalgae successful development it is first necessary that the bacteria be adapted to the SWW characteristics (Fouilland et al., 2018). The heterotrophic bacteria development consumes the excess organic compounds in the medium, releasing inorganic carbon, a preferred assimilation source for microalgae in mixotrophic cultivation, and enabling this group re-establishment (Zhan et al., 2017).