Mangrove microbial diversity and the impact of trophic contamination

https://doi.org/10.1016/j.marpolbul.2012.11.015Get rights and content

Abstract

Mangroves are threatened ecosystems that provide numerous ecosystem services, especially through their wide biodiversity, and their bioremediation capacity is a challenging question in tropical areas. In a mangrove in Mayotte, we studied the potential role of microbial biofilm communities in removing nutrient loads from pre-treated wastewater. Microbial community samples were collected from tree roots, sediments, water, and from a colonization device, and their structure and dynamics were compared in two areas: one exposed to sewage and the other not. The samples from the colonization devices accurately reflected the natural communities in terms of diversity. Communities in the zone exposed to sewage were characterized by more green algae and diatoms, higher bacteria densities, as well as different compositions. In the area exposed to sewage, the higher cell densities associated with specific diversity patterns highlighted adapted communities that may play a significant role in the fate of nutrients.

Highlights

► The impact of nutrient increases on biofilm microbial communities is investigated in a tropical mangrove. ► Microbial communities were sampled using a colonization device in the mangrove. ► Their structure and diversity were shaped by the nutrient load level. ► Microbial communities may play a key role in the fate of nutrients.

Introduction

Recent assessments suggest that about one-third of mangrove, sea grass and salt marsh areas around the world have already been lost over recent decades as a result of reclamation, deforestation, engineering and urbanization (Lewis et al., 2011, Peixoto et al., 2011, Penha-Lopes et al., 2011), as well as transformation to provide aquaculture ponds (Alongi, 2002). Many coastal lagoons in the tropics support dense mangrove forests, which are productive areas harboring a wide diversity of organisms. Adapted to intertidal zones, they are subjected to highly variable physicochemical conditions of salinity, flooding, light, and temperature, which give rise to the high diversity that characterizes mangrove ecosystems (Feller et al., 2010).

Mangroves are often established on nutrient-rich sediments, and are able to absorb excess nutrients without suffering any major structural or functional disturbance (Saenger, 2002). Nedwell (1975) was the first to show that pretreated wastewater discharge into a mangrove swamp in Fiji reduced eutrophication in adjacent coastal waters, and therefore suggested that mangroves might serve as the final stage in sewage treatment. Since then, most attempts to evaluate the potential role of mangrove to remove nutrients from sewage have been done in the form of experimental studies (Chu et al., 1998, Wu et al., 2008), or on constructed pilot sites (Yang et al., 2008, Tam et al., 2009). Yang et al. (2008) highlighted the need for complementary treatment to eliminate pathogenic bacteria. However, only a few studies have investigated natural mangrove sites in intertidal zones (Wang et al., 2010, Penha-Lopes et al., 2011). Wang et al. (2010) explored changes in water quality in a subtropical mangrove estuary (China), and highlighted the fact that large quantities of nutrients may be trapped by the mangrove during flood periods. In a comparison of non-impacted and peri-urban subtropical mangroves (Mozambique), Penha-Lopes et al. (2011) showed that both the structure and the fitness of a natural shrimp population (Palaemon concinnus) were impacted by nutrient levels. Tam showed as early as (1998) that adding wastewater to mangrove soils seems to stimulate the growth of microbial populations, probably because of the nutrients and carbon supplied in wastewater, but this compartment has not been thoroughly explored within the framework of domestic-sewage discharge in mangroves. Estuarine waters are dynamic environments in which sediments, and marine and fresh water mix, resulting in salinity and nutrient gradients. Shifts in physical, chemical, and microbiological properties between freshwater and adjacent coastal marine environments occur over short periods of time, driven by tides and freshwater flows, which create an intense abiotic pressure that influences the composition of bacterioplankton communities (Crump et al., 1999). Microorganisms have large population sizes and display long dispersal distances, high reproductive rates, and remarkable genetic diversity, suggesting that they can cross environmental boundaries, including salinity, more readily than multicellular organisms (Logares et al., 2009).

On solid surfaces, microorganisms organize themselves into microbial biofilms, mainly consisting of heterotrophic bacteria and autotrophic eukaryotes that are often known collectively as the “microphytobenthos”, which is embedded in a microbial organic matrix (Decho, 2000). These biofilm communities are present in the upper layers of sediment (Holguin et al., 2001) as well as on tree roots (Toledo et al., 1995, Gomes et al., 2010), where they carry out a number of different functions, including nutrient transformation, sediment stabilization, plant-growth promotion, and even providing protected suitable areas for pathogens entering marine systems. The impacts of pollutants such as polycyclic aromatic hydrocarbons (PAH, for a review see Fernandez-Luqueno et al. (2011)) and phthalates have been studied in mangrove ecosystems. Conversely, changes in trophic conditions due to nutrient loading have received much less investigation in these tropical zones (Underwood, 2002, Ramanathan et al., 2008), unless they are threatened by urban sewage or aquaculture. Yet such changes, which have been extensively studied in freshwater ecosystems, are known to modify the functionality of biofilm communities, as well as their diversity (e.g. Pesce et al., 2008, Berthon et al., 2011).

This study focuses on biofilm microbial communities in a tropical mangrove with two different trophic statuses, either exposed or not exposed to effluents from a domestic wastewater pre-treatment device. We tested an experimental approach using artificial substrates to collect natural biofilms, in order to avoid sampling biases due to environmental heterogeneity. Microbial communities were also sampled in situ to collect pelagic, benthic and root biofilms in order to compare their structures and diversities. This approach provides a very useful way of extending our knowledge about the microbial communities associated to mangrove ecosystems, and of evaluating the impact of urban sewage on these communities.

Section snippets

Study sites

Two sites in a mangrove located in Chirongui bay, southwest of Mayotte Island in the Indian Ocean (12°55′S, 45°09′E, Fig. 1) were investigated in this study. This area was described in a previous study by Herteman (2010). Domestic wastewater collected from the contiguous village of Malamani (400-equivalent inhabitants) was subjected to primary treatment in a sedimentation tank which reduced the suspended matter concentration by 50%. Pre-treated wastewater was then discharged at low tide into a

Results

The impacted and reference plots shared common characteristics for temperature (27.4 ± 0.04), pH (6.62 ± 0.03), salinity (34.5 ± 1.5) and cohesive sediment structure, (mostly silt: 76%; fine sand: 21%, clay: 3% at surface). However, they differed with regard to nutrient concentrations (Table 1). In the surface layer of the sediment (0–30 cm), NO3-, NO2- and NH4+ concentrations in the interstitial water were higher in the impacted plot than in reference plot, whereas no difference was observed in the

Discussion

This study reports for the first time the microbial diversity of a mangrove in the tropical island of Mayotte which suffers anthropogenic impacts due to a demographic explosion. The differences found in the community composition add to our knowledge about microbial distribution in mangrove ecosystems. The loading of nutrients in aquatic ecosystems has often been reported to be a cause of functional, structural and diversity changes in biofilm microbenthic communities in freshwater ecosystems

Conclusion

Our results, obtained using a simple and efficient colonization device for microbial communities, give a preliminary insight regarding the impacts of pre-treated wastewater effluents on microbial communities in a mangrove. In particular, a denser bacterial community exhibiting a specific assemblage that may be able to enhance nutrient recycling and consumption, have been observed in the impacted plot. However, further information about these systems is required. Data mining remains necessary,

Acknowledgements

This paper is a contribution to the ECOMET project, funded by the French Ministry of Ecology, Energy, Sustainable Development, and Sea (MEEDDM), Grant No. CV070000783. The experimental site in Chirongui Bay, Mayotte Island, was set up as part of a joint research program between the Water Syndicate of Mayotte (SIEAM) and the Laboratory of Functional Ecology and the Environment (ECOLAB CNRS University of Toulouse), and is partially funded by the Ecological Engineering Program (2007, 2009–2010) of

References (55)

  • D.B. Nedwell

    Inorganic Nitrogen-metabolism in a eutrophicated tropical mangrove estuary

    Water Research

    (1975)
  • G. Penha-Lopes et al.

    Monitoring anthropogenic sewage pollution on mangrove creeks in southern Mozambique: a test of Palaemon concinnus Dana, 1852 (Palaemonidae) as a biological indicator

    Environmental Pollution

    (2011)
  • S. Pesce et al.

    Longitudinal changes in microbial planktonic communities of a French river in relation to pesticide and nutrient inputs

    Aquatic Toxicology

    (2008)
  • N.F.Y. Tam

    Effects of wastewater discharge on microbial populations and enzyme activities in mangrove soils

    Environmental Pollution

    (1998)
  • N.F.Y. Tam et al.

    Novel technology in pollutant removal at source and bioremediation

    Ocean and Coastal Management

    (2009)
  • M. Troussellier et al.

    Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids

    Fems Microbiology Ecology

    (1999)
  • M. Wang et al.

    Maintenance of estuarine water quality by mangroves occurs during flood periods: a case study of a subtropical mangrove wetland

    Marine Pollution Bulletin

    (2010)
  • Y. Wu et al.

    Constructed mangrove wetland as secondary treatment system for municipal wastewater

    Ecological Engineering

    (2008)
  • Q. Yang et al.

    Potential use of mangroves as constructed wetland for municipal, sewage treatment in Futian, Shenzhen, China

    Marine Pollution Bulletin

    (2008)
  • D.M. Alongi

    Present state and future of the world’s mangrove forests

    Environmental Conservation

    (2002)
  • R.I. Amann et al.

    Combination of 16S ribosomal-RNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial-populations

    Applied and Environmental Microbiology

    (1990)
  • T. Amano et al.

    Contribution of anammox bacteria to benthic nitrogen cycling in a mangrove forest and shrimp ponds, Haiphong, Vietnam

    Microbes and Environments

    (2011)
  • V. Berthon et al.

    Using diatom life-forms and ecological guilds to assess organic pollution and trophic level in rivers: a case study of rivers in south-eastern France

    Hydrobiologia

    (2011)
  • T. Bouvier et al.

    A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems

    Environmental Microbiology

    (2007)
  • B.K.K. Chan et al.

    Patterns of biofilm succession on a sheltered rocky shore in Hong Kong

    Biofouling

    (2003)
  • D.F.R. Cleary et al.

    Assessment of variation in bacterial composition among microhabitats in a mangrove environment using DGGE fingerprints and barcoded pyrosequencing

    Plos One

    (2012)
  • B.C. Crump et al.

    Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean

    Applied and Environmental Microbiology

    (1999)
  • Cited by (23)

    • Mangrove microbial community recovery and their role in early stages of forest recolonization within shrimp ponds

      2023, Science of the Total Environment
      Citation Excerpt :

      Mangroves microbial communities can also remove antibiotic resistance genes (ARGs) from the surrounding environment, even when mangroves are frequently exposed to high loads of antibiotics (Imchen et al., 2018; Liu et al., 2020; Zhao et al., 2019). Despite its ecological and socioeconomic relevance, mangrove forests have been impacted by multiple global and local-scale stressors, such as sea-level rise, deforestation, sedimentation, unplanned dam projects, land reclamation, overfishing, and pollution through sewage release or oil and trace metal inputs (Alongi, 2008; Bouchez et al., 2013; Dos Santos et al., 2011; Lewis et al., 2011). The causes leading mangrove deforestation are related to agriculture and aquaculture implementations, including shrimp farming (Friess et al., 2019).

    • Two new species of mud dragons (Scalidophora: Kinorhyncha) inhabiting a human-impacted mangrove from Mayotte (Southwestern Indian Ocean)

      2022, Zoologischer Anzeiger
      Citation Excerpt :

      Several studies verified that Kinorhyncha density is negatively impacted when the amount of organic matter strongly increases due to domestic sewage or aquatic farms (e.g. Santos et al., 2009; Capdeville et al., 2018; Carugati et al., 2018). The increase of organic matter content may initially enhance microbial proliferation (bacteria and microalgae), one of the likely food sources for kinorhynchs, which could be beneficial for these animals (Nomaki et al., 2008; Bouchez et al., 2013; Capdeville et al., 2018). However, it also causes a decrease in the available oxygen and stimulates the formation of hydrogen sulfide, which may explain the negative long-term impact (Ansari et al., 1984; Sutherland et al., 2007; Dal Zotto et al., 2016; Capdeville et al., 2018).

    • Wastewater bioremediation by mangrove ecosystems impacts crab ecophysiology: In-situ caging experiment

      2020, Aquatic Toxicology
      Citation Excerpt :

      As already discussed in Capdeville (2018), the response of the crab community and the individual physiological response may be linked to WW discharge but also to the induced environmental modifications. Indeed, different feedback effects are possible since WW discharges induce major changes in mangrove plants (Herteman et al., 2011) and microbial communities (Bouchez et al., 2013), which are the food source for most of the mangrove crab species. As already demonstrated, eutrophication occurs in the impacted area (Bouchez et al., 2013; Capdeville et al., 2018; Herteman et al., 2011).

    • Microbes from wastewater treated mangrove soil and their heavy metal accumulation and Zn solubilization

      2019, Biocatalysis and Agricultural Biotechnology
      Citation Excerpt :

      The present work also recorded more counts of microbes in the wastewater treated mangrove soil (Fig. 1). This is in accordance with Agnes Bouchez et al. (2013) who have found that the sewage treatment enhances microbial densities and diversity. Similarly Tam (1998) has recorded that total counts of both aerobic and anaerobic heterotrophic bacteria, nitrifiers and denitrifiers in mangrove soils receiving wastewater are significantly higher than those found in the control soils.

    View all citing articles on Scopus
    View full text