Dataset Information

Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh.

ABSTRACT: Microbial metabolism is the engine that drives global biogeochemical cycles, yet many key transformations are carried out by microbial consortia over short spatiotemporal scales that elude detection by traditional analytical approaches. We investigate syntrophic sulfur cycling in the 'pink berry' consortia of the Sippewissett Salt Marsh through an integrative study at the microbial scale. The pink berries are macroscopic, photosynthetic microbial aggregates composed primarily of two closely associated species: sulfide-oxidizing purple sulfur bacteria (PB-PSB1) and sulfate-reducing bacteria (PB-SRB1). Using metagenomic sequencing and (34) S-enriched sulfate stable isotope probing coupled with nanoSIMS, we demonstrate interspecies transfer of reduced sulfur metabolites from PB-SRB1 to PB-PSB1. The pink berries catalyse net sulfide oxidation and maintain internal sulfide concentrations of 0-500??m. Sulfide within the berries, captured on silver wires and analysed using secondary ion mass spectrometer, increased in abundance towards the berry interior, while ?(34) S-sulfide decreased from 6‰ to -31‰ from the exterior to interior of the berry. These values correspond to sulfate-sulfide isotopic fractionations (15-53‰) consistent with either sulfate reduction or a mixture of reductive and oxidative metabolisms. Together this combined metagenomic and high-resolution isotopic analysis demonstrates active sulfur cycling at the microscale within well-structured macroscopic consortia consisting of sulfide-oxidizing anoxygenic phototrophs and sulfate-reducing bacteria.

SUBMITTER: Wilbanks EG

PROVIDER: S-EPMC4262008 | biostudies-literature | 2014 Nov

REPOSITORIES: biostudies-literature

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Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh.

Wilbanks Elizabeth G EG Jaekel Ulrike U Salman Verena V Humphrey Parris T PT Eisen Jonathan A JA Facciotti Marc T MT Buckley Daniel H DH Zinder Stephen H SH Druschel Gregory K GK Fike David A DA Orphan Victoria J VJ

Environmental microbiology 20140226 11

Microbial metabolism is the engine that drives global biogeochemical cycles, yet many key transformations are carried out by microbial consortia over short spatiotemporal scales that elude detection by traditional analytical approaches. We investigate syntrophic sulfur cycling in the 'pink berry' consortia of the Sippewissett Salt Marsh through an integrative study at the microbial scale. The pink berries are macroscopic, photosynthetic microbial aggregates composed primarily of two closely asso ...[more]

PMID: 24428801

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Project description:Microbial interactions driving key biogeochemical fluxes often occur within multispecies consortia that form spatially heterogeneous microenvironments. Here, we describe the "green berry" consortia of the Sippewissett salt marsh (Falmouth, MA, United States): millimeter-sized aggregates dominated by an uncultured, diazotrophic unicellular cyanobacterium of the order Chroococcales (termed GB-CYN1). We show that GB-CYN1 is closely related to Crocosphaera watsonii (UCYN-B) and "Candidatus Atelocyanobacterium thalassa" (UCYN-A), two groups of unicellular diazotrophic cyanobacteria that play an important role in marine primary production. Other green berry consortium members include pennate diatoms and putative heterotrophic bacteria from the Alphaproteobacteria and Bacteroidetes. Tight coupling was observed between photosynthetic oxygen production and heterotrophic respiration. When illuminated, the green berries became supersaturated with oxygen. From the metagenome, we observed that GB-CYN1 encodes photosystem II genes and thus has the metabolic potential for oxygen production unlike UCYN-A. In darkness, respiratory activity rapidly depleted oxygen creating anoxia within the aggregates. Metagenomic data revealed a suite of nitrogen fixation genes encoded by GB-CYN1, and nitrogenase activity was confirmed at the whole-aggregate level by acetylene reduction assays. Metagenome reads homologous to marker genes for denitrification were observed and suggest that heterotrophic denitrifiers might co-occur in the green berries, although the physiology and activity of facultative anaerobes in these aggregates remains uncharacterized. Nitrogen fixation in the surface ocean was long thought to be driven by filamentous cyanobacterial aggregates, though recent work has demonstrated the importance of unicellular diazotrophic cyanobacteria (UCYN) from the order Chroococcales. The green berries serve as a useful contrast to studies of open ocean UCYN and may provide a tractable model system to investigate microbial dynamics within phytoplankton aggregates, a phenomenon of global importance to the flux of particulate organic carbon and nitrogen in surface waters.

Project description:Motile phototrophic consortia are highly regular associations in which numerous cells of green sulfur bacteria surround a flagellated colorless beta-proteobacterium in the center. To date, seven different morphological types of such consortia have been described. In addition, two immotile associations involving green sulfur bacteria are known. By employing a culture-independent approach, different types of phototrophic consortia were mechanically isolated by micromanipulation from 14 freshwater environments, and partial 16S rRNA gene sequences of the green sulfur bacterial epibionts were determined. In the majority of the lakes investigated, different types of phototrophic consortia were found to co-occur. In all cases, phototrophic consortia with the same morphology from the same habitat contained only a single epibiont phylotype. However, morphologically indistinguishable phototrophic consortia collected from different lakes contained different epibionts. Overall, 19 different types of epibionts were detected in the present study. Whereas the epibionts within one geographic region were very similar (Dice coefficient, 0.582), only two types of epibionts were found to occur on both the European and North American continents (Dice coefficient, 0.190). None of the epibiont 16S rRNA gene sequences have been detected so far in free-living green sulfur bacteria, suggesting that the interaction between epibionts and chemotrophic bacteria in the phototrophic consortia is an obligate interaction. Based on our phylogenetic analysis, the epibiont sequences are not monophyletic. Thus, the ability to form symbiotic associations either arose independently from different ancestors or was present in a common ancestor prior to the radiation of green sulfur bacteria and the transition to the free-living state in independent lineages. The present study thus demonstrates that there is great diversity and nonrandom geographical distribution of phototrophic consortia in the natural environment.

Project description:A dense population of the phototrophic consortium "Pelochromatium roseum" was investigated in the chemocline of a temperate holomictic lake (Lake Dagow, Brandenburg, Germany). Fluorescence in situ hybridization revealed that the brown epibionts of "P. roseum" constituted up to 37% of the total bacterial cell number and up to 88% of all green sulfur bacteria present in the chemocline. Specific amplification of 16S rRNA gene fragments of green sulfur bacteria and denaturing gradient gel electrophoresis fingerprinting yielded a maximum of four different DNA bands depending on the year of study, indicating that the diversity of green sulfur bacteria was low. The 465-bp 16S rRNA gene sequence of the epibiont of "P. roseum" was obtained after sorting of individual consortia by micromanipulation, followed by a highly sensitive PCR. The sequence obtained represents a new phylotype within the radiation of green sulfur bacteria. Maximum light-dependent H(14)CO(3)(-) fixation in the chemocline in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea suggested that there was anaerobic autotrophic growth of the green sulfur bacteria. The metabolism of the epibionts was further studied by determining stable carbon isotope ratios (delta(13)C) of their specific biomarkers. Analysis of photosynthetic pigments by high-performance liquid chromatography revealed the presence of high concentrations of bacteriochlorophyll (BChl) e and smaller amounts of BChl a and d and chlorophyll a in the chemocline. Unexpectedly, isorenieratene and beta-isorenieratene, carotenoids typical of other brown members of the green sulfur bacteria, were absent. Instead, four different esterifying alcohols of BChl e were isolated as biomarkers of green sulfur bacterial epibionts, and their delta(13)C values were determined. Farnesol, tetradecanol, hexadecanol, and hexadecenol all were significantly enriched in (13)C compared to bulk dissolved and particulate organic carbon and compared to the biomarkers of purple sulfur bacteria. The difference between the delta(13)C values of farnesol, the major esterifying alcohol of BChl e, and CO(2) was -7.1%, which provides clear evidence that the mode of growth of the green sulfur bacterial epibionts of "P. roseum" in situ is photoautotrophic.

Dataset Information

Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh.

Publications

Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh.

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