Search bioRxiv⌕ Search

Biology subjects

Garczarek, L.

Publications and source records attributed to Garczarek, L..

4 recordsLinked to original sources

Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies

The ever-increasing number of available microbial genomes and metagenomes provide new opportunities to investigate the links between niche partitioning and genome evolution in the ocean, notably for the abundant and ubiquitous marine picocyanobacteria Prochlorococcus and Synechococcus. Here, by combining metagenome analyses of the Tara Oceans dataset with comparative genomics, including phyletic patterns and genomic context of individual genes from 256 reference genomes, we first showed that picocyanobacterial communities thriving in different niches possess distinct gene repertoires. We then managed to identify clusters of adjacent genes that display specific distribution patterns in the field (CAGs) and are thus potentially involved in the adaptation to particular environmental niches. Several CAGs are likely involved in the uptake or incorporation of complex organic forms of nutrients, such as guanidine, cyanate, cyanide, pyrimidine or phosphonates, which might be either directly used by cells, for e.g. the biosynthesis of proteins or DNA, or degraded into inorganic nitrogen and/or phosphorus forms. We also highlight the frequent presence of CAGs involved in polysaccharide capsule biosynthesis in Synechococcus populations thriving in both nitrogen- and phosphorus-depleted areas, which are absent in low-iron regions, suggesting that the complexes they encode may be too energy-consuming for picocyanobacteria thriving in these areas. In contrast, Prochlorococcus populations thriving in iron-depleted areas specifically possess an alternative respiratory terminal oxidase, potentially involved in the reduction of Fe(III) into Fe(II). Together, this study provides insights into how these key members of the phytoplankton community might behave in response to ongoing global change. Significance StatementPicocyanobacteria face various environmental conditions in the ocean and numerous studies have shown that genetically distinct ecotypes colonize different niches. Yet the functional basis of their adaptation remains poorly known, essentially due to the large number of genes of yet unknown function, many of which have little or no beneficial effect on fitness. Here, by combining comparative genomics and metagenomics approaches, we have identified not only single genes but also entire gene clusters, potentially involved in niche adaptation. Although being sometimes present in only one or a few sequenced strains, they occur in a large part of the population in specific ecological niches and thus constitute precious targets for elucidating the biochemical function of yet unknown niche-related genes.

microbiology↗

Comparative thermophysiology of marine Synechococcus CRD1 strains isolated from different thermal niches in iron-depleted areas

Marine Synechococcus cyanobacteria are ubiquitous in the ocean, a feature likely related to their extensive genetic diversity. Amongst the major lineages, clades I and IV preferentially thrive in temperate and cold, nutrient-rich waters, whilst clades II and III prefer warm, nitrogen or phosphorus-depleted waters. The existence of such cold (I/IV) and warm (II/III) thermotypes is corroborated by physiological characterization of representative strains. A fifth clade, CRD1, was recently shown to dominate the Synechococcus community in iron-depleted areas of the world ocean and to encompass three distinct ecologically significant taxonomic units (ESTUs CRD1A-C) occupying different thermal niches, suggesting that distinct thermotypes could also occur within this clade. Here, using comparative thermophysiology of strains representative of these three CRD1 ESTUs we show that the CRD1A strain MITS9220 is a warm thermotype, the CRD1B strain BIOS-U3-1 a cold temperate thermotype, and the CRD1C strain BIOS-E4-1 a warm temperate stenotherm. Curiously, the CRD1B thermotype lacks traits and/or genomic features typical of cold thermotypes. In contrast, we found specific physiological traits of the CRD1 strains compared to their clade I, II, III and IV counterparts, including a lower growth rate and photosystem II maximal quantum yield at most temperatures and a higher turnover rate of the D1 protein. Together, our data suggests that the CRD1 clade prioritizes adaptation to low-iron conditions over temperature adaptation, even though the occurrence of several CRD1 thermotypes likely explains why the CRD1 clade as a whole occupies most iron-limited waters.

microbiology↗

Global phylogeography of marine Synechococcus in coastal areas reveals strikingly different communities than in the open ocean

Marine Synechococcus comprise a numerically and ecologically prominent phytoplankton group, playing a major role in both carbon cycling and trophic networks in all oceanic regions except in the polar oceans. Despite their high abundance in coastal areas, our knowledge of Synechococcus communities in these environments is based on only a few local studies. Here, we use the global metagenome dataset of the Ocean Sampling Day (June 21st 2014) to get a snapshot of the taxonomic composition of coastal Synechococcus communities worldwide, by recruitment on a reference database of 141 picocyanobacterial genomes, representative of the whole Prochlorococcus, Synechococcus and Cyanobium diversity. This allowed us to unravel drastic community shifts over small to medium scale gradients of environmental factors, in particular along European coasts. The combined analysis of the phylogeography of natural populations and the thermophysiological characterization of eight strains, representative of the four major Synechococcus lineages (clades I to IV), also brought novel insights about the differential niche partitioning of clades I and IV, which most often co-dominate the Synechococcus community in cold and temperate coastal areas. Altogether, this study tackles the main differences between open-ocean and coastal communities worldwide.

microbiology↗

Diversity and evolution of pigment types and the phycobilisome rod gene region of marine Synechococcus cyanobacteria

Synechococcus picocyanobacteria are ubiquitous and abundant photosynthetic organisms in the marine environment and contribute for an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon, based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examined the variability of gene sequences and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements including tyrosine recombinases, suggesting that their genomic plasticity relies on a tycheposon-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the rest of the genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of population-scale mechanisms in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events.

microbiology↗