Endolithic chlorophyll d-containing phototrophs

Abstract

Cyanobacteria in the genus Acaryochloris are the only known oxyphototrophs that have exchanged chlorophyll a (Chl a) with Chl d as their primary photopigment, facilitating oxygenic photosynthesis with near infrared (NIR) light. Yet their ecology and natural habitats are largely unknown. We used hyperspectral and variable chlorophyll fluorescence imaging, scanning electron microscopy, photopigment analysis and DNA sequencing to show that Acaryochloris-like cyanobacteria thrive underneath crustose coralline algae in a widespread endolithic habitat on coral reefs. This finding suggests an important role of Chl d-containing cyanobacteria in a range of hitherto unexplored endolithic habitats, where NIR light-driven oxygenic photosynthesis may be significant.

Figure 1

Endolithic habitat of Chl d -containing cyanobacteria. (a) Typical Chl d-containing yellow–greenish biofilm found directly under encrusting coralline algae. Labels indicate two different areas of interest (AOI) where pulse-amplitude modulated (PAM) variable chlorophyll fluorescence imaging was carried out: (1) Endolith AOI is dominated by filamentous cyanobacteria and green algae, and (2) Chl d AOI is dominated by Acaryochloris-like Chl d-containing cyanobacteria. Another circular AOI indicates a Chl d-containing area where no PAM analysis was carried out. Inserts show scanning electron microscopy pictures for the respective AOI; note the presence of round 1–2 μm large bacteria, similar in size and shape to Acaryochloris marina. (b) Hyperspectral reflectance image at 710 nm, that is, the peak absorbance of Chl d in situ. Dark areas indicate strong Chl d absorption. (c) Reflectance spectra of the two AOI showing distinct spectral signatures of Chl d around 710 nm. (d) Photosynthetic activity versus irradiance measured as the PSII related relative electron transport rate (rETR) in the two AOI.

Figure 2

Scanning electron microscopy and hyperspectral measurements performed on a dead coral sample with the crustose coralline algal layer removed. (a) Biofilm found under encrusting coralline algae. (b) Reflectance spectra extracted from hyperspectral imaging of three AOI in (a) showing Chl d absorption around 710 nm. (c–f) Scanning electron microscopy pictures portraying biofilms growing below encrusting corraline algae. Note frequent occurrence of 1–2 μm large A. marina like cells (c–f), along with filamentous cyanobacteria (c, d) and Ostreobium-like filamentous green algae (e).