Influence of local climate and climate change on aeroterrestrial phototrophic biofilms

Aeroterrestrial phototrophic biofilms colonize natural and man-made surfaces and may damage the material they settle on. The occurrence of biofilms varies between regions with different climatic conditions. The aim of this study was to evaluate the influence of meteorological factors on the growth of aeroterrestrial phototrophs. Phototrophic biomass was recorded on roof tiles at six sites within Germany five times over a period of five years and compared to climatic parameters from neighboring weather stations. All correlating meteorological factors influenced water availability on the surface of the roof tiles. The results indicate that the frequency of rainy days and not the mean precipitation per season is more important for biofilm proliferation. It is also inferred that the macroclimate is more important than the microclimate. In conclusion, changed (regional) climatic conditions may determine where in central Europe global change will promote or inhibit phototrophic growth in the future.     

An integrated approach for assessing the bioreceptivity of glazed tiles to phototrophic microorganisms

A laboratory-based methodology was designed to assess the bioreceptivity of glazed tiles. The experimental set-up consisted of multiple steps: manufacturing of pristine and artificially aged glazed tiles, enrichment of phototrophic microorganisms, inoculation of phototrophs on glazed tiles, incubation under optimal conditions and quantification of biomass. In addition, tile intrinsic properties were assessed to determine which material properties contributed to tile bioreceptivity. Biofilm growth and biomass were appraised by digital image analysis, colorimetry and chlorophyll a analysis. SEM, micro-Raman and micro-particle induced X-ray emission analyses were carried out to investigate the biodeteriorating potential of phototrophic microorganisms on the glazed tiles. This practical and multidisciplinary approach showed that the accelerated colonization conditions allowed different types of tile bioreceptivity to be distinguished and to be related to precise characteristics of the material. Aged tiles showed higher bioreceptivity than pristine tiles due to their higher capillarity and permeability. Moreover, biophysical deterioration caused by chasmoendolithic growth was observed on colonized tile surfaces.     

Benthic phototrophic community from Kiran soda lake,south-eastern Siberia

Phototrophic bacterial mats from Kiran soda lake (south-eastern Siberia) were studied using integrated approach including analysis of the ion composition of water, pigments composition, bacterial diversity and the vertical distribution of phototrophic microorganisms in the mats. Bacterial diversity was investigated using microscopic examination, 16S rRNA gene Illumina sequencing and culturing methods. The mats were formed as a result of decomposition of sedimented planktonic microorganisms, among which cyanobacteria of the genus Arthrospira predominated. Cyanobacteria were the largest part of phototrophs in the mats, but anoxygenic phototrophs were significant fraction. The prevailing species of the anoxygenic phototrophic bacteria are typical for soda lakes. The mats harbored aerobic anoxygenic phototrophic bacteria, purple sulfur and non-sulfur bacteria, as well as new filamentous phototrophic Chloroflexi. New strains of Thiocapsa sp. Kir-1, Ectothiorhodospira sp. Kir-2 and Kir-4, Thiorhodospira sp. Kir-3 and novel phototrophic Chloroflexi bacterium Kir15-3F were isolated and identified.

     

Ciliates as engineers of phototrophic biofilms

1. Phototrophic biofilms consist of a matrix of phototrophs, non‐photosynthetic bacteria and extracellular polymeric substances (EPS) which is spatially structured. Despite widespread exploitation of algae and bacteria within phototrophic biofilms, for example by protozoans, the ‘engineering’ effects of these ciliates on the spatial heterogeneity of phototrophic biofilms are poorly studied. 2. We studied the potential engineering effects of two ciliates, Urostyla sp. and Paramecium bursaria, on the spatial heterogeneity of synthetic multispecies biofilms. Biomass of phototrophic organisms, EPS and bacteria was analysed three dimensionally using confocal laser scanning microscopy. Spatial heterogeneity and cover of the phototrophs, bacteria and EPS were determined at several depths within the biofilm. 3. Ciliate species did not interfere with the overall development of phototrophic microorganisms, because the thickness of the biofilm was equal whether the ciliates were present or not, even though their abundance did affect spatial heterogeneity of biofilm components. When Urostyla was present, it reduced aggregation in EPS and bacteria and increased EPS biovolume. This implies a local facilitating effect of ciliates on photosynthetic activity. Biofilms to which Paramecium was added did not differ from controls in terms of phototrophs, EPS cover and biovolume. Nevertheless, ciliates affected the spatial heterogeneity of these components as phototrophs and EPS became more evenly distributed. 4. This study shows that ecosystem engineering by organisms does not only occur at large spatial scales, as in grasslands and estuaries, but also plays a role at the microscopic scale of biofilms. This effect on spatial heterogeneity was not driven by substantial exploitation of biofilm components, but via the subtle engineering effects of ciliates.     

Phototrophic biofilms and their potential applications

Phototrophic biofilms occur on surfaces exposed to light in a range of terrestrial and aquatic environments. Oxygenic phototrophs like diatoms, green algae, and cyanobacteria are the major primary producers that generate energy and reduce carbon dioxide, providing the system with organic substrates and oxygen. Photosynthesis fuels processes and conversions in the total biofilm community, including the metabolism of heterotrophic organisms. A matrix of polymeric substances secreted by phototrophs and heterotrophs enhances the attachment of the biofilm community. This review discusses the actual and potential applications of phototrophic biofilms in wastewater treatment, bioremediation, fish-feed production, biohydrogen production, and soil improvement.     

Comparison of cultivation-dependent and molecular methods for studying the diversity of anoxygenic purple phototrophs in sediments of an eutrophic brackish lagoon

Phototrophic anoxygenic purple bacteria play a key role in many aquatic ecosystems by oxidizing sulfur compounds and low-molecular-weight organic compounds using light as energy source. In this study, molecular methods based upon pufM gene (photosynthetic unit forming gene) were compared with culture-dependent methods to investigate anoxygenic purple phototrophic communities in sediments of an eutrophic brackish lagoon. Thirteen strains, belonging to eight different genera of purple phototrophic bacteria were isolated with a large dominance of the metabolically versatile purple non-sulfur bacteria (eight strains), some purple sulfur bacteria (three strains) and two strains belonging to the Roseobacter clade (aerobic phototrophs). The pufM genes amplified from the isolated strains were not detected by the molecular methods [terminal-restriction fragment length polymorphism (T-RFLP)] applied on in situ communities. An environmental clone library of the pufM gene was thus constructed from sediment samples. The results showed that most of the clones probably corresponded to aerobic phototrophic bacteria. Our results demonstrate that the culture-dependent techniques remain the best experimental approach for determining the diversity of phototrophic purple non-sulfur bacteria whereas the molecular approach clearly illustrated the abundance of organisms related to the Roseobacter clade in these eutrophic sediments.     

Light environment and synthesis of bacteriochlorophyll by populations of Chromatium okenii under natural environmental conditions

Abstract: In the meromictic alpine Lake Cadagno a dense layer of phototrophic bacteria, mainly Chromatium okenii and Amoebobacter purpureus , develop annually at the chemocline at about 10 to 11 m depth. Radiometric spectral profiles of the incident sunlight demonstrate different attenuation coefficients in the mixolimnion and in the chemocline not only for the visible light effective at each depth (photosynthetically available radiation), but also for selected photosynthetically active wavelengths used by oxygenic and anoxygenic phototrophs. Phototrophic bacteria sampled from the upper part of the layer at the maximum of cell concentration were incubated in transparent bottles at the sampling depth and at a lower depth where the light intensity is only a few percent of the one at the sampling depth. Within 4 h the specific bacteriochlorophyll concentration (Bchl protein⁻¹) increased up to 50% depending on the difference in light intensity between the sampling and the incubation depth. The specific bacteriochlorophyll concentration in the upper part of the layer remained constant (53.0 mg Bchl g⁻¹ protein, S.D. = 4.8) in spite of large changes in cell concentrations in the lake water over the season. These observations illustrate the phenomenon of light-regulated pigment synthesis under natural conditions.     

Phototrophic plankton of siderotrophic meromictic Lake Kuznechikha (Republic Mari El,Russia)

During summer thermal stratification, a broad transition zone with hypoxic conditions is formed in meromictic ferruginous Lake Kuznechikha between the thermocline and the main gradient of water mineralization. In this zone, the chemical composition of water undergoes an ecologically significant transformation due to overlapping gradients of nutrient concentrations and redox conditions. We present an analysis of a strongly vertically structured community of prokaryotic and eukaryotic phototrophs developing in the lake as a whole and especially in the transition zone. In early summer 2009, a sequence of phototrophic organisms with depth in order Chlorophyceae → Chromatiales → Chloroflexales → Euglenales → Chlorobiales was observed in the transition zone, while cyanobacteria were almost completely absent. Biomass maximum of anoxygenic phototrophic bacteria was located between the peaks of phototrophic picoplankton and euglenoids. Such a coexistence of oxygenic and anoxygenic phototrophs in a wide range of depths is highly unusual and sharply distinguishes Lake Kuznechikha from waterbodies with sulphide-containing monimolimnion.     

Simultaneous methanogenesis and phototrophic bacterial growth in relatively dry sewage sludge under light

Anaerobically digested sewage sludge with a variety of moisture content, namely 81%, 86%, 90% and 98%, were anaerobically cultured at 35 degrees C under light. Phototrophic bacteria grew in the 86% moisture sludge (bacteriochlorophyll a, 0.46 g/L), 90% sludge (bacteriochlorophyll a, 0.36 g/L) and 98% sludge (bacteriochlorophyll a, 0.04 g/L) with methane production. Phototrophic bacteria could not grow in the 81% moisture sludge (bacteriochlorophyll a 0.004 g/L). Phototrophic bacteria could assimilate about 46% of the extracellular ammonium in the 90% moisture sludge. Phototrophic bacteria utilized organic compounds competing with methanogens; therefore, methane yield from the 90% moisture sludge under the light conditions was lower than that under the dark conditions. Phototrophic bacteria could grow in anaerobically digested sludge with relatively low moisture content, and assimilated extracellular ammonium in the sludge. The quality of digested sludge with phototrophic bacterial biomass for fertilizer could be improved compared with that without phototrophic bacterial biomass.     

Trophic status of <Emphasis Type="Italic">Chlamydomonas reinhardtii</Emphasis> influences the impact of iron deficiency on photosynthesis

To investigate the impact of iron deficiency on bioenergetic pathways in Chlamydomonas, we compared growth rates, iron content, and photosynthetic parameters systematically in acetate versus CO₂-grown cells. Acetate-grown cells have, predictably (2-fold) greater abundance of respiration components but also, counter-intuitively, more chlorophyll on a per cell basis. We found that phototrophic cells are less impacted by iron deficiency and this correlates with their higher iron content on a per cell basis, suggesting a greater capacity/ability for iron assimilation in this metabolic state. Phototrophic cells maintain both photosynthetic and respiratory function and their associated Fe-containing proteins in conditions where heterotrophic cells lose photosynthetic capacity and have reduced oxygen evolution activity. Maintenance of NPQ capacity might contribute to protection of the photosynthetic apparatus in iron-limited phototrophic cells. Acetate-grown iron-limited cells maintain high growth rates by suppressing photosynthesis but increasing instead respiration. These cells are also able to maintain a reduced plastoquinone pool.     

Partitioning of CO2 Incorporation Among Planktonic Microbial Guilds and Estimation of In Situ Specific Growth Rates

Partitioning of CO₂ incorporation into oxygenic phototrophic, anoxygenic phototrophic, and chemolithoautotrophic guilds was determined in a freshwater lake (Lake Cisó, Banyoles, Spain). CO₂ incorporation into the different types of microorganisms was studied at different depths, during diel cycles, and throughout the year. During winter holomixis, the whole lake became anoxic and both the anoxygenic and chemolithoautotrophic guilds were more active at the surface of the lake, whereas the activity of the oxygenic guild was negligible. During stratification, the latter guild was more active in the upper metalimnion, whereas the anoxygenic guild was more active in the lower metalimnion. Specific growth rates and doubling times were estimated for the most conspicuous phototrophic microorganisms. Doubling times for Cryptomonas phaseolus ranged between 0.5 and 192 days, whereas purple sulfur bacteria (Chromatiaceae-like) ranged between 1.5 and 238 days. These growth rates were similar to those calculated with a different approach in previous papers and indicate slow-growing populations with very large biomass. Overall, the annual total CO₂ incorporation in Lake Cisó was 220 g C m⁻². Most of the CO₂ incorporation, however, was due to the chemolithoautotrophic guild (61% during holomixis and 56% during stratification), followed by the anoxygenic phototrophic guild (35 and 19%, respectively) and the oxygenic phototrophs (4 and 25%, respectively), making dark carbon fixation the key process in the autotrophic metabolism of the lake.     

Populations of Anaerobic Phototrophic Bacteria in a Spartina alterniflora Salt Marsh

Habitat-simulating media were used with the Hungate anaerobic roll tube technique to enumerate culturable anaerobic photosynthetic bacteria in sediment, tidal waters, and Spartina alterniflora plant samples collected from the salt marsh at Sapelo Island, Ga. No phototrophs were detected in samples of creekside (low marsh) sediment or in tidal waters in creekside regions. In the high marsh region, 90% of anaerobic phototrophic bacteria occurred in the top 5 mm of sediment and none were detected below 6 mm. There was a seasonal variation, with maximal populations occurring in summer and fall (mean, 4.4 × 10⁵ phototrophs g of dry sediment⁻¹) and minimal numbers occurring in winter (mean, 3.9 × 10³ phototrophs g of dry sediment⁻¹). During winter and late spring, phototrophs had a patchy distribution over the high marsh sediment surface. In contrast, during late summer they had a random uniform distribution. Tidal water collected over high marsh sediment contained an average of 8.7 × 10² phototrophs ml⁻¹, with no significant seasonal variation. Anaerobic phototrophic bacteria were also cultured from the lower stem tissue of S. alterniflora growing in both the high (4.3 × 10⁴ phototrophs g of dry tissue⁻¹) and creekside (4.9 × 10⁴ phototrophs g of dry tissue⁻¹) marsh regions. Chromatium buderi, Chromatium vinosum, Thiospirillum sanguineum, Rhodospirillum molischianum, and Chlorobium phaeobacteroides were the predominant anaerobic phototrophic species cultured from high marsh sediment. The two Chromatium species were dominant.     

Algal and Cyanobacterial Biofilms on Calcareous Historic Buildings

Major microorganisms in biofilms on external surfaces of historic buildings are algae, cyanobacteria, bacteria, and fungi. Their growth causes discoloration and degradation. We compared the phototrophs on cement-based renderings and limestone substrates at 14 historic locations (47 sites sampled) in Europe and Latin America. Most biofilms contained both cyanobacteria and algae. Single-celled and colonial cyanobacteria frequently constituted the major phototroph biomass on limestone monuments (32 sites sampled). Greater numbers of phototrophs, and especially of algae and of filamentous morphotypes, were found on cement-based renderings (15 sites), probably owing to the porosity and small pore size of the latter substrates, allowing greater entry and retention of water. All phototrophic groups were more frequent on Latin American than on European buildings (20 and 27 sites, respectively), with cyanobacteria and filamentous phototrophs showing the greatest differences. The results confirm the influence of both climate and substrate on phototroph colonization of historic buildings. Received: 7 March 2002 / Accepted: 8 April 2002     

Phototrophic bacterial production of oleic acid in an illuminated upflow anaerobic sludge blanket reactor

Phototrophic bacterial cells in the effluent from a lighted upflow anaerobic sludge blanket reactor supplied with a medium containing 142 mg S (as SO₄ ^2–) l^–1 accumulated a 6.8% w/w oleic acid content in cells and 19 mg cell-bound oleic acid l^–1 in the effluent. Pure cultures of Rhodopseudomonas palustris and Blastochloris sulfoviridis isolated from the effluent also accumulated 5.1 and 6.4% w/w oleic acid contents in cells, respectively. The oleic acid content in the cells recovered from the LUASB reactor effluent was related to the phototrophic bacterial population in the LUASB reactor. The inverse relationship was observed in the LUASB reactor between phototrophic bacterial growth and sulfate concentration in the influent.     

Cryopreservation of anoxygenic phototrophic Fe(II)-oxidizing bacteria

Preservation and storage of microbial stock cultures is desirable since the risk of contamination or loss of living cultures is immanent while over long periods mutations accumulate. Generally, it is rather difficult to preserve photosynthetic bacteria due to their sensitive photosynthetic membranes [1]. Phototrophic Fe(II)-oxidizing bacteria face an additional challenge; since they are exposed to light and Fe(II) during growth, they have to cope with radicals from Fenton reactions of Fe(II)-species, light and water. Therefore, phototrophic Fe(II)-oxidizing strains are thought to be especially susceptible to genetic modifications. Here, we provide a simple and fast protocol using glycerol as cryo-protectant to cryopreserve three strains of anoxygenic phototrophic Fe(II)-oxidizing bacteria from different taxa: α-proteobacteria, γ-proteobacteria and chloroflexi. All three strains investigated could be revived after 17 months at −72 °C. This suggests that a long-term storage of phototrophic Fe(II)-oxidizing strains is possible.     

Peatland microhabitat heterogeneity drives phototrophic microbe distribution and photosynthetic activity

Phototrophic microbes are widespread in soils, but their contribution to soil carbon (C) uptake remains underexplored in most terrestrial systems, including C-accreting systems such as peatlands. Here, by means of metabarcoding and ecophysiological measurements, we examined how microbial photosynthesis and its biotic (e.g., phototrophic community structure, biomass) and abiotic drivers (e.g., Sphagnum moisture, light intensity) vary across peatland microhabitats. Using a natural gradient of microhabitat conditions from pool to forest, we show that the structure of phototrophic microbial communities shifted from a dominance of eukaryotes in pools to prokaryotes in forests. We identified five groups of co-occurring phototrophic operational taxonomic units with specific environmental preferences across the gradient. Along with such structural changes, we found that microbial C uptake was the highest in the driest and shadiest microhabitats. This study renews and improves current views on phototrophic microbes in peatlands, as the contribution of microbial photosynthesis to peatland C uptake has essentially been studied in wet microhabitats.     

Plasmid transfer and susceptibility to antibiotics in the halophilic phototrophs Rhodovibrio salinarum and Rhodothalassium salexigens

The present study defines a series of genetic procedures to be used for molecular studies in photosynthetic halophilic species such as Rhodovibrio salinarum and Rhodothalassium salexigens. In both species, the minimal inhibitory concentrations for the antibiotics tetracycline, rifampicin, chloramphenicol, spectinomycin, streptomycin, and kanamycin were determined. In addition, conjugal transfer of IncP and IncQ plasmids from Escherichia coli was demonstrated and the resistance markers expressed in these halophiles were determined. Finally, Rth. salexigens growth dependence on variable salt concentrations was measured: maximal growth rates were seen at 6% and 4% NaCl under phototrophic and chemotrophic conditions, respectively. To the best of our knowledge, this is the first report analyzing the genetic properties of two representative species of halophilic purple non-sulfur phototrophs.     

Differences of the protozoan biomass and grazing during spring and summer in the Indian sector of the Southern Ocean

The dynamics of protozoa were investigated during two cruises in the Indian sector of the Southern Ocean: the early spring ANTARES 3 cruise (28 September to 8 November 1995) and the late summer ANTARES 2 cruise (6 February to 8 March 1994). Biomass and feeding activity of protozoa were measured as well as the biomass of their potential prey – bacteria and phototrophic flagellates – along the 62°E meridian. The sampling grid extended from the Polar Frontal region to the Coastal and Continental Shelf Zone in late summer and to the ice edge in spring, crossing the Antarctic Divergence. Protozoan biomass, although low in absolute terms, contributed 30% and 20% to the total microbial biomass (bacteria, phytoplankton and protozoa) in early spring and late summer, respectively. Nanoprotozoa dominated the total protozoan biomass. The geographical and seasonal distribution of protozoan biomass was correlated with that of phototrophic flagellates. However, bacterial and phototrophic flagellate biomass were inversely correlated. Phototrophic flagellates dominated in the Sea Ice Zone whereas bacteria were predominant at the end of summer in the Polar Frontal region and Coastal and Continental Shelf Zone. Furthermore, bacteria were the most important component of the microbial community (57% of the total microbial biomass) in late summer. Phototrophic flagellates were ingested by both nano-and microprotozoa. In contrast, bacteria were only ingested by nanoprotozoa. Protozoa controlled up to 90% of the daily bacterial production over the period examined. The spring daily protozoan ingestion controlled more than 100% of daily phototrophic flagellate production. This control was less strong at the end of summer when protozoan grazing controlled 42% of the daily phototrophic flagellate production. Accepted: 30 October 1999     

Comparative study of metabolism of the purple photosynthetic bacteria grown in the light and in the dark under anaerobic and aerobic conditions

For three species of anoxygenic phototrophic alphaproteobacteria differing in their reaction to oxygen and light, physiological characteristics (capacity for acetate assimilation, activity of the tricarboxylic acid (TCA) cycle enzymes, respiration, and the properties of the oxidase systems) were studied. Nonsulfur purple bacteria Rhodobacter sphaeroides, Rhodobaca bogoriensis, and aerobic anoxygenic phototrophic bacteria Roseinatronobacter thiooxidans were the subjects of investigation. All of these organisms were able to grow under aerobic conditions in the dark using the respiratory system with cytochrome aa ₃ as the terminal oxidase. They differed, however, in their capacity for growth in the light, bacteriochlorophyll synthesis, and regulation of activity of the TCA cycle enzymes. Oxygen suppressed bacteriochlorophyll synthesis by Rha. sphaeroides and Rbc. bogoriensis both in the dark and in the light. Bacteriochlorophyll synthesis in Rna. thiooxidans occurred only in the dark and was suppressed by light. The results on acetate assimilation by the studied strains reflected the degree of their adaptation to aerobic growth in the dark. Acetate assimilation by light-grown Rha. sphaeroides was significantly higher than by the dark-grown ones. Unlike Rha. sphaeroides, acetate assimilation by Rbc. bogoriensis in the light under anaerobic and aerobic conditions was much less dependent on the growth conditions. Aerobic acetate assimilation by all studied bacteria was promoted by light. In Rha. sphaeroides, activity of the TCA cycle enzymes increased significantly in the cells grown aerobically in the dark. In Rbc. bogoriensis, activity of most of the TCA cycle enzymes under aerobic conditions either decreased or remained unchanged. Our results confirm the origin of modern chemoorganotrophs from anoxygenic phototrophic bacteria. The evolution from anoxygenic photoorganotrophs to aerobic chemoorganotrophs included several stages: nonsulfur purple bacteria → nonsulfur purple bacteria similar to Rbc. bogoriensis → aerobic anoxygenic phototrophs → chemoorganotrophs.