Multiple losses of photosynthesis in Nitzschia (Bacillariophyceae)

Abstract

Summary In order to obtain insights into the evolution of colorless (apochlorotic) diatoms, we investigated newly established apochlorotic strains of Nitzschia spp. using light and electron microscopy and molecular phylogenetic analyses. Fluorescence microscopic observations demonstrated that the apochlorotic diatoms lack chlorophylls. Transmission electron microscopy of two apochlorotic strains also demonstrated that their plastids lacked thylakoids; instead, having four‐membrane‐bound organelles without thylakoids, similar to nonphotosynthetic plastid remnants. From the apochlorotic strains, we also found plastid small subunit rRNA genes that were unusually long branched in phylogenetic analyses, as observed in other nonphotosynthetic plastids. Molecular phylogenetic analysis of the nucleus‐encoded large subunit rRNA genes showed eight distinct lineages for apochlorotic diatoms. The eight apochlorotic lineages were not monophyletic, suggesting that the loss of photosynthesis took place multiple times independently within Nitzschia. Several diatoms, including Nitzschia spp., are mixotrophic, which is an expected mode of nutrition that would help explain the evolutionary switch from a photosynthetic lifestyle to a heterotrophic lifestyle.

Growth characterization of non-photosynthetic diatoms, <i>Nitzschia</i> spp., inhabiting estuarine mangrove forests of Ishigaki Island, Japan

“…Identification was performed by morphological observation under light microscopy according to the criteria reported in Kamikawa et al (2015a). All strains were observed using an inverted microscope (Olympus IX70, Tokyo, Japan) equipped with a FLOYD multi interface digital camera (WRAYMER, Osaka, Japan).…”

“…Strains used in this study. Lineages were identified with morphology and LSU rRNA gene sequences according to Kamikawa et al (2015a). Growth rates estimated at 30°C during the logarithmic growth phase within 48 h after inoculation are shown.…”

“…The diatom genus Nitzschia is benthic and is comprised of more than 1,000 species, containing 6 non-photosynthetic species (Guiry & Guiry 2017, Lewin & Lewin 1967, Li & Volcani 1987. Our previous phylogenetic analyses suggested that the loss of photosynthesis in Nitzschia has happened multiple times independently (Kamikawa et al 2015a). Transmission electron microscopy revealed that some of these species have retained non-photosynthetic plastid structures with reduced thylakoids.…”

“…This evaporation phenomenon also triggers other severe conditions such as high temperature and high salinity. Nevertheless, it has been reported that various algal species are capable of inhabiting such severe environments (Williams 1964, Mizuno 1992, Colijn & van Buurt 1975, Admiraal & Peletier 1980, Pinckney & Zingmark 1991, Kamikawa et al 2015a.…”

“…We have investigated the diversity of non-photosynthetic diatoms (Kamikawa et al 2015a). We isolated and established non-photosynthetic diatom strains from the tidal estuarine areas of mangroves in the Ryukyu Islands, Japan.…”