Loïc Charpy

Cyanobacteria in Coral Reef Ecosystems: A Review

Cyanobacteria have dominated marine environments and have been reef builders on Earth for more than three million years (myr). Cyanobacteria still play an essential role in modern coral reef ecosystems by forming a major component of epiphytic, epilithic, and endolithic communities as well as of microbial mats. Cyanobacteria are grazed by reef organisms and also provide nitrogen to the coral reef ecosystems through nitrogen fixation. Recently, new unicellular cyanobacteria that express nitrogenase were found in the open ocean and in coral reef lagoons. Furthermore, cyanobacteria are important in calcification and decalcification. All limestone surfaces have a layer of boring algae in which cyanobacteria often play a dominant role. Cyanobacterial symbioses are abundant in coral reefs; the most common hosts are sponges and ascidians. Cyanobacteria use tactics beyond space occupation to inhibit coral recruitment. Cyanobacteria can also form pathogenic microbial consortia in association with other microbes on living coral tissues, causing coral tissue lysis and death, and considerable declines in coral reefs. In deep lagoons, coccoid cyanobacteria are abundant and are grazed by ciliates, heteroflagellates, and the benthic coral reef community. Cyanobacteria produce metabolites that act as attractants for some species and deterrents for some grazers of the reef communities.

Physical and chemical control of the phytoplankton of Ahe lagoon, French Polynesia.

The environmental characteristics of Ahe deep lagoon (Tuamotu Archipelago, French Polynesia) were studied over 3 years with the aim of explaining the spatial and temporal variability of the natural food available for pearl oysters with a special focus on phytoplankton biomass and global photosynthesis/respiration ratio of the lagoon. Chlorophyll averaged 0.34±0.01 μg L(-1) and our findings did not confirm increased phytoplankton biomass in deep lagoonal waters. Phytoplankton production appears to be limited firstly by nitrogen and respiratory processes overpass photosynthetic processes at least in the north-eastern edge of the atoll. Grazing by pearl oysters in culture seems to decrease the POC concentration but not the phytoplankton biomass. Oysters graze mainly on non chlorophyllian particles.

Spatio-temporal diversity of free-living and particle-attached prokaryotes in the tropical lagoon of Ahe atoll (Tuamotu Archipelago) and its surrounding oceanic waters

Spatio-temporal variability of prokaryotic water column communities inside and outside a Polynesian tropical lagoon subjected to pearl oysters farming was assessed in terms of abundance by quantitative PCR and diversity by DGGE. Communities and operational taxonomic units (OTUs) were analysed according to dry/rainy seasons and free-living/particle-attached state. Bacterial density was higher in the lagoon compared to ocean and a seasonal trend was observed. No influence of the localisation within lagoon or of the planktonic/attached states was noticed on bacterial abundance and diversity. The OTUs belonged to Cyanobacteria, to heterotrophic groups in Proteobacteria and Flavobacteria. Archaeal abundance showed seasonal tendency and particle-prevalence, but no effect of lagoon or oceanic location was observed. Lagoon and oceanic archaeal diversity were different and Euryarchaeota (MG-II, MBG, and Halobacteria) were detected. During the dry season, planktonic and particle-associated community differed, whereas at rainy season, both communities were similar and included members usually associated with coral.

Metazooplankton communities in the Ahe atoll lagoon (Tuamotu Archipelago, French Polynesia): Spatiotemporal variations and trophic relationships

Metazooplankton abundance, biomass (<80 μm, 200-500 μm and >500 μm) and community structure in the Ahe atoll were studied together with their relationships with environmental factors (temperature, salinity, wind) and trophic factors (phytoplankton, bacteria, heterotrophic nanoflagellates (HNF) and ciliates) during three periods in 2008-2009. Meroplankton, mainly bivalve and gastropod larvae, was dominant. Holoplankton was dominated by copepods, the main species being Oithona spp., Paracalanus parvus, Clausocalanus spp., Corycaeus spp., Acartia fossae and Undinula vulgaris. The results suggest a clear wind influence on the structure and horizontal distribution of the zooplankton communities. The metazooplankton appeared to be controlled mainly by food resources, suggesting a bottom-up control. The low nanophytoplankton biomass in contrast to the high abundance of picophytoplankton, HNF and nano-particle grazers (mainly Oithona spp., Paracalanus and bivalve larvae) highlighted the importance of the microbial loop in the food web.

Factors influencing microbial mat composition, distribution and dinitrogen fixation in three western Indian Ocean coral reefs

Cyanobacteria have been found to be important for primary production and nitrogen supply on coral reefs. Here, the distribution of cyanobacteria that dominate microbial mats (identified by using microscopic and molecular tools), their abundance, and specific contributions and timing of N2 fixation, were studied in two coral reef systems of the western Indian Ocean: Mayotte (Comoros) and Tulear (Toliara, Madagascar). The results were compared with previously published data from the reefs of La Réunion Island (Mascarenes). Variations in nutrient levels, temperature and light penetration (Secchi) were also measured and compared. The reefs in Mayotte are situated in oligotrophic ocean waters and support coral reefs in good condition. The reef of Tulear was overgrown by algae. The shallow lagoon and reef in La Réunion showed signs of eutrophication and coral degradation. All three reefs maintained a diverse population of benthic cyanobacterial mats. A total of 13 different cyanobacterial morphotypes were encountered, belonging mainly to the genera Anabaena, Hydrocoleum, Leptolyngbya and Lyngbya (as identified by morphotypes and 16 S RNA analyses), but with variable abundances. Twelve of the 13 dominant cyanobacteria observed in the three sites fixed dinitrogen with daily rates of up to 42 nmol N2 µg−1 Chl a. Maximum values were achieved by the heterocystous Anabaena sp. during daylight in Mayotte, which exhibited strongly light‐stimulated nitrogenase activity. Mats dominated by non‐heterocystous cyanobacteria fixed both during daylight and the night, with daily rates up to 38 nmol N2 µg−1 Chl a (by Lyngbya majuscula, Mayotte). Hydrocoleum‐dominated mats fixed N2 at rates between 0 (H. glutinosum, Tulear) and 23.4 nmol N2 µg−1 Chl a (H. coccineum, Mayotte). Cyanobacteria are normal constituents of the benthic microflora in tropical regions, but their abundance, diversity and species composition changes with environmental conditions and so do the rates of N2 fixation on the lagoon floors.

Spatial and temporal dynamics of size-structured photosynthetic parameters (PAM) and primary production (13C) of pico- and nano-phytoplankton in an atoll lagoon

Atoll lagoons display a high diversity of trophic states due mainly to their specific geomorphology, and probably to their level and mode of human exploitation. We investigated the functioning of the Ahe atoll lagoon, utilized for pearl oyster farming, through estimations of photosynthetic parameters (pulse amplitude modulation fluorometry) and primary production ((13)C incorporation) measurements of the size structured phytoplankton biomass (<2 μm and >2 μm). Spatial and temporal scales of variability were surveyed during four seasons, over 16 months, at four sites within the lagoon. While primary production (P) was dominated by the picophytoplankton, its biomass specific primary productivity (P(B)) was lower than in other atoll lagoons. The variables size fraction of the phytoplankton, water temperature, season, the interaction term station*fraction and site, explained significantly the variance of the data set using redundancy analysis. No significant trends over depth were observed in the range of 0-20 m. A clear spatial pattern was found which was persistent over the seasons: south and north sites were different from the two central stations for most of the measured variables. This pattern could possibly be explained by the existence of water cells showing different water residence time within the lagoon. Photoacclimation strategies of the two size fractions differed through their light saturation coefficient (higher for picophytoplankton), but not through their maximum photosynthetic capacity (ETR(max)). Positive linear relationships between photosynthetic parameters indicated that their dynamic was independent of light availability in this ecosystem, but most probably dependent on nutrient availability and/or rapid changes in the community structure. Spatial and temporal patterns of the measured processes are then further discussed in the context of nutrient availability and the possible role of cultured oysters in nutrient recycling.

Do human activities affect the picoplankton structure of the Ahe atoll lagoon (Tuamotu Archipelago, French Polynesia)?

The spatial variations of the picoplankton (photoautotrophic and heterotrophic microorganisms) in the Ahe atoll lagoon were studied in May and October 2008 to assess whether they were affected by human activities along the atoll. Spatial patterns were studied using 10 sampling stations chosen according to the location of the anthropogenic activities (pearl farming, harbor). Experiments were also carried out to determine whether bacterial growth, with or without predators, was limited by inorganic (N and P) substrates. The results showed that heterotrophic bacterioplankton abundance was superior to the photoautotrophic organisms, especially in May. Significant increases in bacterial abundance were observed in May after 24 h incubation with +P and +N (but not in October). All samples complied with the quality levels for fecal indicator bacteria (FIB) defined by the European Union and there was no evidence that human sewage had any impact on picoplankton over the whole atoll.

Morphological, genetic and physiological characterization of Hydrocoleum, the most common benthic cyanobacterium in tropical oceans

ABSTRACT Populations of the benthic diazotrophic cyanobacterium Hydrocoleum Kützing (1843) are widely distributed in coral reefs and lagoons of tropical oceans, where they contribute to benthic nitrogen fixation. We compared the morphological, molecular and physiological features of 31 freshwater and marine Hydrocoleum populations from geographically different localities and five specimens from herbaria. Our aims were to compare the features of Hydrocoleum with the morphologically and phylogenetically related genera Trichodesmium Ehrenberg ex Gomont 1892 and Blennothrix Kützing 1843, and to provide the basis for the validity of the genus Hydrocoleum. The Hydrocoleum populations were distributed over a wide range of sizes, showing no consistent inter-population grouping and leaving no gaps between groups that were traditionally attributed to different species. Transmission electron microscopy showed regular cell division rhythms in all Hydrocoleum populations with each cell division completed before the next one was initiated, similar to that described for Trichodesmium. In contrast, Blennothrix populations exhibited multiple initiation of cross-wall formation. Most Hydrocoleum populations fixed nitrogen at consistently higher nightly rates. The phylogenetic analysis of 16S rRNA and nifH gene sequences placed all morphologically distinct Hydrocoleum and Trichodesmium populations within a tight cluster. Neither of the analysed genes brought any further resolution of phenotypically and ecologically distinguished forms. However, freshwater morphospecies of Blennothrix together with the type species Blennothrix vermicularis Kützing were separated from the Trichodesmium/Hydrocoleum cluster, which further supported the genotypic distinction between the compared taxa, in addition to the fact that they also differ in morphology and ecology. We concluded that the genus Hydrocoleum possesses unique features that warrant its maintenance in the botanical classification system and that its introduction in bacteriological manuals as a valid cyanobacterial genus is acceptable.