Nonlinear effect of irradiance on photoheterotrophic activity and growth of the aerobic anoxygenic phototrophic bacterium Dinoroseobacter shibae

Abstract

Aerobic anoxygenic photosynthetic bacteria are an important component of marine microbial communities. They produce energy in light using bacteriochlorophyll a containing photosystems. This extra energy provides an advantage over purely heterotrophic bacteria. One of the most intensively studied AAP bacteria is Dinoroseobacter shibae, a member of the environmentally important Roseobacter clade. Light stimulates its growth and metabolism, but the effect of light intensity remains unclear. Here, we show that an increase in biomass along an irradiance gradient followed the exponential rise to the maximum curve, with saturation at about 300 µmol photons m s , without any inhibition at light intensities up to 600 µmol photons m s . The cells adapted to higher irradiance by reducing pigmentation and increasing the electron transfer rate. This additional energy allowed D. shibae to redirect the metabolism of organic carbon sources such as glucose, leucine, glutamate, acetate and pyruvate toward anabolism, resulting in a twofold increase of their assimilation rates. We provide equations that can be feasibly incorporated into the existing model of D. shibae metabolism to further advance our understanding of the role of photoheterotrophy in the ocean.

Extended temperature optimum of photosynthetic reaction centers in Rhodobacterales

“…shibae grown between 15 and 45°C. To remove the inhibitory effect of light on pigment synthesis observed previously (Piwosz et al 2018), we incubated all the cultures in the dark. The best growth was observed in cultures grown between 30 and 40°C, with the maximum growth rate (~ 3.4 d -1 ) and biomass obtained at 35°C (Fig.…”

“…The single cell contains ca. 3,000 reaction centers (Piwosz et al 2018) that represent moderately pigmented cells when compared with the values of ~ 150-30,000 RC per cell found in a representative sample of purple nonsulfur and AAP bacteria by Selyanin et al (2016). The investigated species living in the aquatic environments where they are exposed mostly to the blue-green light spectrum (infra-red part of the spectrum is rapidly removed in the water column).…”

Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment

“…Such conditions favor bacterial groups with higher growth efficiency, such as AAP bacteria (41). The competitive advantage of photoheterotrophic AAP bacteria over purely heterotrophic bacteria is enhanced with increasing irradiance, because AAP bacteria significantly reduce their respiration rates when producing ATP via energy absorbed on photosystems (26,27). This may explain the higher bacterial growth rates in the OL-Inh treatment despite the lower carbon availability.…”

“…These organisms utilize energy from light for ATP synthesis but require organic carbon for growth (25). AAP bacteria produce ATP on bacteriochlorophyll-containing reaction centers in the process of cyclic photophosphorylation (25), and this additional energy allows them to reduce the requirement for oxidative phosphorylation (respiration), thus increasing their growth efficiency (26,27). AAP bacteria represent the metabolically more active part of aquatic bacterial communities, presumably consuming a large fraction of phytoplankton-derived DOC (28,29).…”

Determining lineage-specific bacterial growth curves with a novel approach based on amplicon reads normalization using internal standard (ARNIS)

“…The growth rate can be directly determined in microbial cultures as the relative change of biomass (frequently approximated by microscopy counts) per unit of time [ 3 , 4 ]. Despite the fact that laboratory experiments provide invaluable information on bacterial growth and physiology [ 5 , 6 ], they cannot be directly applied in natural planktonic communities, where a fraction of the biomass is constantly removed at lineage-specific rates by protozoan grazing, viral lysis, or UV damage [ 7 , 8 ]. Therefore, in situ bacterial specific growth rates are typically determined using manipulation experiments, in which mortality is reduced using pre-filtration and/or dilution, and the growth is followed by microscopy [ 9 ].…”