Abstract
The aim of this study was to investigate the planktonic and the holobiont Madracis decactis (Scleractinia) microbial diversity along a turbulence-driven upwelling event, in the world's most isolated tropical island, St Peter and St Paul Archipelago (SPSPA, Brazil). Twenty one metagenomes were obtained for seawater (N = 12), healthy and bleached holobionts (N = 9) before, during and after the episode of high seawater turbulence and upwelling. Microbial assemblages differed between low turbulence-low nutrient (LLR) and high-turbulence-high nutrient (HHR) regimes in seawater. During LLR there was a balance between autotrophy and heterotrophy in the bacterioplankton and the ratio cyanobacteria:heterotrophs ~1 (C:H). Prochlorales, unclassified Alphaproteobacteria and Euryarchaeota were the dominant bacteria and archaea, respectively. Basic metabolisms and cyanobacterial phages characterized the LLR. During HHR C:H < < 0.05 and Gammaproteobacteria approximated 50% of the most abundant organisms in seawater. Alteromonadales, Oceanospirillales, and Thaumarchaeota were the dominant bacteria and archaea. Prevailing metabolisms were related to membrane transport, virulence, disease, and defense. Phages targeting heterotrophs and virulence factor genes characterized HHR. Shifts were also observed in coral microbiomes, according to both annotation–indepent and -dependent methods. HHR bleached corals metagenomes were the most dissimilar and could be distinguished by their di- and tetranucleotides frequencies, Iron Acquision metabolism and virulence genes, such as V. cholerae-related virulence factors. The healthy coral holobiont was shown to be less sensitive to transient seawater-related perturbations than the diseased animals. A conceptual model for the turbulence-induced shifts is put forward.
Highlights
Marine microbial communities are recognized as engines of globally important processes, such as the marine carbon, nitrogen and sulfur cycles (Falkowski et al, 2008; Fuhrman, 2009)
Average Karlin distances for pairs of seawater samples Sw14, -15, -18 and -22 defined three categories based on δ ranges. (i) δ < 11 grouped pairs 1414 and 22-22, indicating high degree of genetic similarity; (ii) 11 < δ < 30 grouped pairs 15–15, 18–18, 14–15, 14–22, and 15–22, indicating intermediate genetic similarity, and (iii) δ > 30 grouped pairs 14–18, 15–18, and 18–22, indicating low genetic similarity
We further investigated the iron uptake system, which is a nonspecific virulence system related to competition skills, and suitable to reflect the overall heterotrophic community
Summary
Marine microbial communities are recognized as engines of globally important processes, such as the marine carbon, nitrogen and sulfur cycles (Falkowski et al, 2008; Fuhrman, 2009). A model of turbulence-nutrients regimes decoupled characteristics and adaptations of phytoplankton assemblages and how they relate to food web structure: (i) high turbulence—low nutrients: low biomass, slow turnover, adaptations for efficient use of light and nutrients (e.g., iron-limited, high latitude waters); (ii) LLR: smaller cells, high turnover, competition for nutrients, retention by recycling (microbial loop); (iii) low turbulence— high nutrients: larger cells, higher biomass, slower turnover, selective pressure to sequester nutrients and minimize losses (e.g., noxious toxic blooms); and (iv) HHR: larger cells, higher biomass, transient, and self-limiting selection for rapid growth (e.g., diatoms) According to this model, the microbial loop is present in all regimes but it dominates the biomass in the low turbulence—high nutrients regime (Cullen et al, 2002)
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