Microbial Diversity and Cyanobacterial Production in Dziani Dzaha Crater Lake, a Unique Tropical Thalassohaline Environment

PLoS One. 2017 Jan 3;12(1):e0168879. doi: 10.1371/journal.pone.0168879. eCollection 2017.

Abstract

This study describes, for the first time, the water chemistry and microbial diversity in Dziani Dzaha, a tropical crater lake located on Mayotte Island (Comoros archipelago, Western Indian Ocean). The lake water had a high level of dissolved matter and high alkalinity (10.6-14.5 g L-1 eq. CO32-, i.e. 160-220 mM compare to around 2-2.5 in seawater), with salinity up to 52 psu, 1.5 higher than seawater. Hierarchical clustering discriminated Dziani Dzaha water from other alkaline, saline lakes, highlighting its thalassohaline nature. The phytoplankton biomass was very high, with a total chlorophyll a concentration of 524 to 875 μg chl a L-1 depending on the survey, homogeneously distributed from surface to bottom (4 m). Throughout the whole water column the photosynthetic biomass was dominated (>97% of total biovolume) by the filamentous cyanobacteria Arthrospira sp. with a straight morphotype. In situ daily photosynthetic oxygen production ranged from 17.3 to 22.2 g O2 m-2 d-1, consistent with experimental production / irradiance measurements and modeling. Heterotrophic bacterioplankton was extremely abundant, with cell densities up to 1.5 108 cells mL-1 in the whole water column. Isolation and culture of 59 Eubacteria strains revealed the prevalence of alkaliphilic and halophilic organisms together with taxa unknown to date, based on 16S rRNA gene analysis. A single cloning-sequencing approach using archaeal 16S rDNA gene primers unveiled the presence of diverse extremophilic Euryarchaeota. The water chemistry of Dziani Dzaha Lake supports the hypothesis that it was derived from seawater and strongly modified by geological conditions and microbial activities that increased the alkalinity. Dziani Dzaha has a unique consortium of cyanobacteria, phytoplankton, heterotrophic Eubacteria and Archaea, with very few unicellular protozoa, that will deserve further deep analysis to unravel its uncommon diversity. A single taxon, belonging to the genus Arthrospira, was found responsible for almost all photosynthetic primary production.

MeSH terms

  • Biodiversity*
  • Biomass
  • Carbon / chemistry
  • Chlorophyll / metabolism
  • Chlorophyll A
  • Cluster Analysis
  • Comoros
  • Cyanobacteria*
  • Geography
  • Hydrogen-Ion Concentration
  • Islands
  • Lakes / microbiology*
  • Models, Statistical
  • Nitrogen / chemistry
  • Oxygen / analysis
  • Oxygen / chemistry
  • Photosynthesis
  • Phytoplankton
  • Principal Component Analysis
  • RNA, Ribosomal, 16S / metabolism
  • Temperature
  • Water Microbiology*

Substances

  • RNA, Ribosomal, 16S
  • Chlorophyll
  • Carbon
  • Nitrogen
  • Oxygen
  • Chlorophyll A

Grants and funding

This work was supported by Université de Montpellier, www.umontpellier.fr, projects METTRO and MYPROBE (CL); Agence Nationale de la Recherche (France), http://www.agence-nationale-recherche.fr, grant n° ANR-13-BS06-0001 (CL); and Total Corporate Foundation, project DZAHA (CL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.