Elsevier

Chemosphere

Volume 211, November 2018, Pages 449-455
Chemosphere

Short communication
Influence of bacteria on the response of microalgae to contaminant mixtures

https://doi.org/10.1016/j.chemosphere.2018.07.161Get rights and content

Highlights

  • The presence of bacteria in the culture medium negatively affected microalgae growth.

  • The absence of bacteria resulted in short term microalgae response to metals and pesticides at low dose.

  • Metals and pesticides were not toxic to microalgae when growing with bacteria.

Abstract

When microalgae are exposed to contaminants, the role of associated bacteria within the phycosphere, the microenvironment surrounding algal cells, remains largely unknown. The present study investigated the importance of algae-associated bacteria on the responses of microalgae growth to metallic and organic toxicant exposure. The effects of a polluted sediment elutriate, and of metal or pesticide mixtures at environmentally relevant concentrations (<10 μg L−1) were assessed on the growth of two microalgae strains: Isochrysis galbana, a prymnesiophyte, and Thalassiosira delicatula, a centric diatom. Both cultures were maintained as axenic or bacterized under similar conditions in batch cultures. In axenic conditions, the metal mixture addition at low concentrations alleviated limitation of growth by metals for T. delicatula relative to control, but inhibited I. galbana growth at highest concentration. In similar axenic conditions, both T. delicatula and I. galbana growth were negatively inhibited by pesticide mixture at concentrations as low as 10 ng L−1. The bacterial diversities associated with the two microalgae strains were significantly different (Bray–Curtis dissimilarity greater than 0.9) but their impact on microalgae growth was similar. The presence of bacteria reduced algal growth rate by ca. 50% compared to axenic cultures, whereas no significant effect of sediment elutriate, metal or pesticide mixtures was noticed on non-axenic algal growth rates. These results show that bacteria may have a negative effect on algal growth but can reduce pesticide toxicity or metal availability to algae.

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.

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