Microenvironmental Ecology of the Chlorophyll b-Containing Symbiotic Cyanobacterium Prochloron in the Didemnid Ascidian Lissoclinum patella

Abstract

The discovery of the cyanobacterium Prochloron was the first finding of a bacterial oxyphototroph with chlorophyll (Chl) b, in addition to Chl a. It was first described as Prochloron didemni but a number of clades have since been described. Prochloron is a conspicuously large (7–25 μm) unicellular cyanobacterium living in a symbiotic relationship, primarily with (sub-) tropical didemnid ascidians; it has resisted numerous cultivation attempts and appears truly obligatory symbiotic. Recently, a Prochloron draft genome was published, revealing no lack of metabolic genes that could explain the apparent inability to reproduce and sustain photosynthesis in a free-living stage. Possibly, the unsuccessful cultivation is partly due to a lack of knowledge about the microenvironmental conditions and ecophysiology of Prochloron in its natural habitat. We used microsensors, variable chlorophyll fluorescence imaging and imaging of O2 and pH to obtain a detailed insight to the microenvironmental ecology and photobiology of Prochloron in hospite in the didemnid ascidian Lissoclinum patella. The microenvironment within ascidians is characterized by steep gradients of light and chemical parameters that change rapidly with varying irradiances. The interior zone of the ascidians harboring Prochloron thus became anoxic and acidic within a few minutes of darkness, while the same zone exhibited O2 super-saturation and strongly alkaline pH after a few minutes of illumination. Photosynthesis showed lack of photoinhibition even at high irradiances equivalent to full sunlight, and photosynthesis recovered rapidly after periods of anoxia. We discuss these new insights on the ecological niche of Prochloron and possible interactions with its host and other microbes in light of its recently published genome and a recent study of the overall microbial diversity and metagenome of L. patella.

Down under the tunic: bacterial biodiversity hotspots and widespread ammonia-oxidizing archaea in coral reef ascidians

“…Many of these symbiont lineages are primarily hostassociated (i.e., obligate symbionts) and represent novel microbial taxa from species level (e.g., Synechococcus spongiarum in sponges, Usher et al, 2004) to phylum level, (e.g., Poribacteria, Fieseler et al, 2004) while others exist in both freeliving and host-associated states, (i.e., facultative symbionts) though generally enriched in the invertebrate microhabitat and rare in seawater communities (Sunagawa et al, 2010). The phylogenetic diversity of symbiotic microbes is associated with a diversity of metabolic pathways in the carbon, (Wilkinson, 1983) nitrogen (Hoffmann et al, 2009) and sulfur cycles (Hoffmann et al, 2005), spurred by the utilization of host waste products (e.g., ammonia), the presence of dimethylsulfoniopropionate (DMSP, Raina et al, 2010) and physico-chemical conditions of the host microenvironment (e.g., oxygen gradients; Hoffmann et al, 2008;Kü hl et al, 2012). The structural and functional diversity of symbiotic microbial communities indicate that invertebrate hosts provide fertile microbial niches that contribute to prokaryotic biodiversity and nutrient cycling in coastal marine ecosystems.…”

“…A growing body of literature suggests that ascidian-associated microbes may play a critical role in the metabolic needs of their host, Martínez-García et al, 2008;Kü hl et al, 2012), yet the microbial communities inhabiting most ascidian species remain unknown. The advent of high-throughput, next-generation DNA sequencing platforms offers new opportunities for in-depth microbial diversity evaluation across large sample sets.…”

Molecular and functional ecology of aquatic microbial symbionts

“…The next two articles evaluate the role of symbionts of an ascidian (Kühl et al, 2012) and a coral (Wangpraseurt et al, 2012) in photosynthetic activities in relation to environmental parameters such as irradiation, periods of anoxia, and physiology of the host. Kühl et al (2012) focus on a chlorophyll b -containing symbiotic cyanobacterium and its photosynthetic activity, whereas Wangpraseurt et al (2012) examine optical microniches in corals and provide evidence for the importance of such microniches for photobiology and stress response of the corals, as well as for the phenotypic and genotypic plasticity of the coral symbionts.…”

“…Kühl et al (2012) focus on a chlorophyll b -containing symbiotic cyanobacterium and its photosynthetic activity, whereas Wangpraseurt et al (2012) examine optical microniches in corals and provide evidence for the importance of such microniches for photobiology and stress response of the corals, as well as for the phenotypic and genotypic plasticity of the coral symbionts.…”

Molecular and functional ecology of aquatic microbial symbionts

“…Kühl et al (2012) focus on a chlorophyll b-containing symbiotic cyanobacterium and its photosynthetic activity, whereas Wangpraseurt et al (2012) examine optical microniches in corals and provide evidence for the importance of such microniches for photobiology and stress response of the corals, as well as for the phenotypic and genotypic plasticity of the coral symbionts.…”