Dating the cyanobacterial ancestor of the chloroplast

Cyanobacteria have played a pivotal role in the history of life on Earth being the first organism to carry out oxygenic photosynthesis, which changed atmospheric chemistry and allowed the evolution of Eukarya. Chloroplasts are the cellular organelles of photoautotrophic eukaryotes in which photosynthesis is conducted. Although the initial suggestion from Mereschkowsky (1905) that cyanobacteria are the ancestors of chloroplasts was greeted with skepticism, the idea is now widely accepted. Here we attempt to resolve and date the cyanobacterial ancestry of the chloroplast using phylogenetic analysis and molecular clocks, because until now, the long-standing question of, from which, among the vast diversity of cyanobacteria, did chloroplasts evolve, has not been resolved. We found that chloroplasts form a monophyletic lineage, are most closely related to subsection I, N2-fixing unicellular cyanobacteria (Order Chroococcales), and heterocyst-forming Order Nostocales cyanobacteria are their sister group. The appearance of Nostocales and of Chroococcales occurred during the Paleoproterozoic, and chloroplasts appeared in the mid-Proterozoic. The capability of N2-fixation in cyanobacteria appeared once during the late Archaen and early Proterozoic eons. Furthermore, we found that oxygen-evolving cyanobacteria could have appeared in the Archean. Our results suggest that a free-living cyanobacterium with the capacity to store starch via oxygenic CO2 fixation, and to fix atmospheric N2, would be a very important intracellular acquisition, which, as can be recounted today from several lines of evidence, would have become the chloroplast by endosymbiosis

Symbiotic unicellular cyanobacteria fix nitrogen in the Arctic Ocean.

Biological dinitrogen (N2) fixation is an important source of nitrogen (N) in low-latitude open oceans. The unusual N2-fixing unicellular cyanobacteria (UCYN-A)/haptophyte symbiosis has been found in an increasing number of unexpected environments, including northern waters of the Danish Straight and Bering and Chukchi Seas. We used nanoscale secondary ion mass spectrometry (nanoSIMS) to measure 15N2 uptake into UCYN-A/haptophyte symbiosis and found that UCYN-A strains identical to low-latitude strains are fixing N2 in the Bering and Chukchi Seas, at rates comparable to subtropical waters. These results show definitively that cyanobacterial N2 fixation is not constrained to subtropical waters, challenging paradigms and models of global N2 fixation. The Arctic is particularly sensitive to climate change, and N2 fixation may increase in Arctic waters under future climate scenarios

Hopanoid lipids may facilitate aerobic nitrogen fixation in the ocean.

Cyanobacterial diazotrophs are considered to be the most important source of fixed N2 in the open ocean. Biological N2 fixation is catalyzed by the extremely O2-sensitive nitrogenase enzyme. In cyanobacteria without specialized N2-fixing cells (heterocysts), mechanisms such as decoupling photosynthesis from N2 fixation in space or time are involved in protecting nitrogenase from the intracellular O2 evolved by photosynthesis. However, it is not known how cyanobacterial cells limit O2 diffusion across their membranes to protect nitrogenase in ambient O2-saturated surface ocean waters. Here, we explored all known genomes of the major marine cyanobacterial lineages for the presence of hopanoid synthesis genes, since hopanoids are a class of lipids that might act as an O2 diffusion barrier. We found that, whereas all non-heterocyst-forming cyanobacterial diazotrophs had hopanoid synthesis genes, none of the marine Synechococcus, Prochlorococcus (non-N2-fixing), and marine heterocyst-forming (N2-fixing) cyanobacteria did. Finally, we conclude that hopanoid-enriched membranes are a conserved trait in non-heterocyst-forming cyanobacterial diazotrophs that might lower the permeability to extracellular O2 This membrane property coupled with high respiration rates to decrease intracellular O2 concentration may therefore explain how non-heterocyst-forming cyanobacterial diazotrophs can fix N2 in the fully oxic surface ocean

In Situ Diazotroph Population Dynamics Under Different Resource Ratios in the North Pacific Subtropical Gyre.

Major advances in understanding the diversity, distribution, and activity of marine N2-fixing microorganisms (diazotrophs) have been made in the past decades, however, large gaps in knowledge remain about the environmental controls on growth and mortality rates. In order to measure diazotroph net growth rates and microzooplankton grazing rates on diazotrophs, nutrient perturbation experiments and dilution grazing experiments were conducted using free-floating in situ incubation arrays in the vicinity of Station ALOHA in March 2016. Net growth rates for targeted diazotroph taxa as well as Prochlorococcus, Synechococcus and photosynthetic picoeukaryotes were determined under high (H) and low (L) nitrate:phosphate (NP) ratio conditions at four depths in the photic zone (25, 45, 75, and 100 m) using quantitative PCR and flow cytometry. Changes in the prokaryote community composition in response to HNP and LNP treatments were characterized using 16S rRNA variable region tag sequencing. Microzooplankton grazing rates on diazotrophs were measured using a modified dilution technique at two depths in the photic zone (15 and 125 m). Net growth rates for most of the targeted diazotrophs after 48 h were not stimulated as expected by LNP conditions, rather enhanced growth rates were often measured in HNP treatments. Interestingly, net growth rates of the uncultivated prymnesiophyte symbiont UCYN-A1 were stimulated in HNP treatments at 75 and 100 m, suggesting that N used for growth was acquired through continuing to fix N2 in the presence of nitrate. Net growth rates for UCYN-A1, UCYN-C, Crocosphaera sp. (UCYN-B) and the diatom symbiont Richelia (associated with Rhizosolenia) were uniformly high at 45 m (up to 1.6 ± 0.5 d-1), implying that all were growing optimally at the onset of the experiment at that depth. Differences in microzooplankton grazing rates on UCYN-A1 and UCYN-C in 15 m waters indicate that the grazer assemblage preyed preferentially on UCYN-A1. Deeper in the water column (125 m), both diazotrophs were grazed at substantial rates, suggesting grazing pressure may increase with depth in the photic zone. Constraining in situ diazotroph growth and mortality rates are important steps for improving parameterization for diazotrophs in global ecosystem models

Temporal variability of diazotroph community composition in the upwelling region off NW Iberia.

Knowledge of the ecology of N2-fixing (diazotrophic) plankton is mainly limited to oligotrophic (sub)tropical oceans. However, diazotrophs are widely distributed and active throughout the global ocean. Likewise, relatively little is known about the temporal dynamics of diazotrophs in productive areas. Between February 2014 and December 2015, we carried out 9 one-day samplings in the temperate northwestern Iberian upwelling system to investigate the temporal and vertical variability of the diazotrophic community and its relationship with hydrodynamic forcing. In downwelling conditions, characterized by deeper mixed layers and a homogeneous water column, non-cyanobacterial diazotrophs belonging mainly to nifH clusters 1G (Gammaproteobacteria) and 3 (putative anaerobes) dominated the diazotrophic community. In upwelling and relaxation conditions, affected by enhanced vertical stratification and hydrographic variability, the community was more heterogeneous vertically but less diverse, with prevalence of UCYN-A (unicellular cyanobacteria, subcluster 1B) and non-cyanobacterial diazotrophs from clusters 1G and 3. Oligotyping analysis of UCYN-A phylotype showed that UCYN-A2 sublineage was the most abundant (74%), followed by UCYN-A1 (23%) and UCYN-A4 (2%). UCYN-A1 oligotypes exhibited relatively low frequencies during the three hydrographic conditions, whereas UCYN-A2 showed higher abundances during upwelling and relaxation. Our findings show the presence of a diverse and temporally variable diazotrophic community driven by hydrodynamic forcing in an upwelling system

Diverse diazotrophs are present on sinking particles in the North Pacific Subtropical Gyre.

Sinking particles transport carbon and nutrients from the surface ocean into the deep sea and are considered hot spots for bacterial diversity and activity. In the oligotrophic oceans, nitrogen (N2)-fixing organisms (diazotrophs) are an important source of new N but the extent to which these organisms are present and exported on sinking particles is not well known. Sinking particles were collected every 6 h over a 2-day period using net traps deployed at 150 m in the North Pacific Subtropical Gyre. The bacterial community and composition of diazotrophs associated with individual and bulk sinking particles was assessed using 16S rRNA and nifH gene amplicon sequencing. The bacterial community composition in bulk particles remained remarkably consistent throughout time and space while large variations of individually picked particles were observed. This difference suggests that unique biogeochemical conditions within individual particles may offer distinct ecological niches for specialized bacterial taxa. Compared to surrounding seawater, particle samples were enriched in different size classes of globally significant N2-fixing cyanobacteria including Trichodesmium, symbionts of diatoms, and the unicellular cyanobacteria Crocosphaera and UCYN-A. The particles also contained nifH gene sequences of diverse non-cyanobacterial diazotrophs suggesting that particles could be loci for N2 fixation by heterotrophic bacteria. The results demonstrate that diverse diazotrophs were present on particles and that new N may thereby be directly exported from surface waters on sinking particles

Genome-scale phylogenetic analysis finds extensive gene transfer among Fungi

Although the role of lateral gene transfer is well recognized in the evolution of bacteria, it is generally assumed that it has had less influence among eukaryotes. To explore this hypothesis we compare the dynamics of genome evolution in two groups of organisms: Cyanobacteria and Fungi. Ancestral genomes are inferred in both clades using two types of methods. First, Count, a gene tree unaware method that models gene duplications, gains and losses to explain the observed numbers of genes present in a genome. Second, ALE, a more recent gene tree-aware method that reconciles gene trees with a species tree using a model of gene duplication, loss, and transfer. We compare their merits and their ability to quantify the role of transfers, and assess the impact of taxonomic sampling on their inferences. We present what we believe is compelling evidence that gene transfer plays a significant role in the evolution of Fungi

Biodiversity and distribution of cyanobacteria at Dronning Maud Land, East Antartica

Biodiversity and distribution of cyanobacteria at Dronning Maud Land, East Antarctica.The current study describes the biodiversity and distribution of cyanobacteria from the natural habitats of Schirmacher land, East Antarctica surveyed during 23rd Indian Antarctic Expedition (2003�2004). Cyanobacteria were mapped using the Global Positioning System (GPS). A total of 109 species (91 species were non-heterocystous and 18 species were heterocystous) from 30 genera and 9 families were recorded; 67, 86 and 14 species of cyanobacteria were identified at altitudes of sea level >100 m, 101�150 m and 398�461 m, respectively. The relative frequency and relative density of cyanobacterial populations in the microbial mats showed that 11 species from 8 genera were abundant and 6 species (Phormidium angustissimum, P. tenue, P. uncinatum Schizothrix vaginata, Nostoc kihlmanii and Plectonema terebrans) could be considered as dominant species in the study area.Biodiversidad y distribución de las cianobacterias de Dronning Maud Land, Antártida Oriental. En este estudio se describe la biodiversidad y distribución de las cianobacterias presentes en los hábitats naturales de Schirmacher, Antártida Oriental, muestreados durante la 23ª Expedición India a la Antártida (2003-2004). Las muestras de cianobacterias fueron georreferenciadas mediante un GPS. Se identificaron 109 especies (91 no heterocistadas y 18 provistas de heterocistes) de 30 géneros y 9 familias; en los tramos de altitud sobre el nivel del mar >100 m, 101-150 m y 398-461 m se detectaron 67, 86 y 14 especies, respectivamente. La frecuencia y densidad relativas de las poblaciones de cianobacterias en los tapices microbianos mostraron que 11 especies de 8 géneros eran abundantes y que 6 especies (Phormidium angustissimum, P. tenue, P. uncinatum, Schizothrix vaginata, Nostoc kihlmanii y Plectonema terebrans) se pueden considerar como dominantes en el área de estudio