Nitrogen fixation has a critical role in marine primary production, yet our understanding of marine nitrogen-fixers (diazotrophs) is hindered by limited observations. Here, we report a quantitative image analysis pipeline combined with mapping of molecular markers for mining >2,000,000 images and >1300 metagenomes from surface, deep chlorophyll maximum and mesopelagic seawater samples across 6 size fractions ( 20 µm). Using imaging and molecular data, we estimate that polyploidy can substantially affect gene abundances of symbiotic versus colony-forming diazotrophs. Our results support the canonical view that larger diazotrophs (>10 μm) dominate the tropical belts, while unicellular cyanobacterial and non-cyanobacterial diazotrophs are globally distributed in surface and mesopelagic layers. We describe co-occurring diazotrophic lineages of different lifestyles and identify high-density regions of diazotrophs in the global ocean. Overall, we provide an update of marine diazotroph biogeographical diversity and present a new bioimaging-bioinformatic workflow. Nitrogen fixation by diazotrophs is critical for marine primary production. Using Tara Oceans datasets, this study combines a quantitative image analysis pipeline with metagenomic mining to provide an improved global overview of diazotroph abundance, diversity and distribution.

/pdf/global-distribution-patterns-of-marine-nitrogen-fixers-by-4gvkmg6sq9.pdf

Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods

Ultra-small microorganisms are ubiquitous in Earth's environments. Ultramicrobacteria, which are defined as having a cell volume of <0.1 μm3, are often numerically dominant in aqueous environments. Cultivated representatives among these bacteria, such as members of the marine SAR11 clade (e.g., "Candidatus Pelagibacter ubique") and freshwater Actinobacteria and Betaproteobacteria, possess highly streamlined, small genomes and unique ecophysiological traits. Many ultramicrobacteria may pass through a 0.2-μm-pore-sized filter, which is commonly used for filter sterilization in various fields and processes. Cultivation efforts focusing on filterable small microorganisms revealed that filtered fractions contained not only ultramicrocells (i.e., miniaturized cells because of external factors) and ultramicrobacteria, but also slender filamentous bacteria sometimes with pleomorphic cells, including a special reference to members of Oligoflexia, the eighth class of the phylum Proteobacteria. Furthermore, the advent of culture-independent "omics" approaches to filterable microorganisms yielded the existence of candidate phyla radiation (CPR) bacteria (also referred to as "Ca. Patescibacteria") and ultra-small members of DPANN (an acronym of the names of the first phyla included in this superphyla) archaea. Notably, certain groups in CPR and DPANN are predicted to have minimal or few biosynthetic capacities, as reflected by their extremely small genome sizes, or possess no known function. Therefore, filtered fractions contain a greater variety and complexity of microorganisms than previously expected. This review summarizes the broad diversity of overlooked filterable agents remaining in "sterile" (<0.2-μm filtered) environmental samples.

/pdf/size-matters-ultra-small-and-filterable-microorganisms-in-3konafstpj.pdf

Size Matters: Ultra-small and Filterable Microorganisms in the Environment.

Biological nitrogen fixation sustains ~50% of ocean primary production. However, our understanding of marine N2-fixers (diazotrophs) is hindered by limited observations. Here, we developed a quantitative image analysis pipeline in concert with mapping of molecular markers for mining >2,000,000 images and >1,300 metagenomes from Tara Oceans, covering surface, deep chlorophyll maximum and mesopelagic layers across 6 organismal size fractions (0-2000 μm). Imaging and molecular data were remarkably congruent. Diazotrophs were detected from ultrasmall bacterioplankton ( 10 μm) dominate the tropical belts, while unicellular diazotrophs were found in surface and mesopelagic samples. Multiple co-occurring diazotrophic lineages were frequently encountered, suggesting that complex overlapping niches are common. Overall, this work provides an updated global snapshot of marine diazotroph biogeographical diversity and highlights new sources and sinks of diazotroph-fueled new production.

/pdf/global-distribution-patterns-of-marine-nitrogen-fixers-by-30m4h4l2kf.pdf

Abstract Background The increased use of metagenomics and single-cell genomics led to the discovery of organisms from phyla with no cultivated representatives and proposed new microbial lineages such as the candidate phyla radiation (CPR or Patescibacteria). These bacteria have peculiar ribosomal structures, reduced metabolic capacities, small genome, and cell sizes, and a general host-associated lifestyle was proposed for the radiation. So far, most CPR genomes were obtained from groundwaters; however, their diversity, abundance, and role in surface freshwaters is largely unexplored. Here, we attempt to close these knowledge gaps by deep metagenomic sequencing of 119 samples of 17 different freshwater lakes located in Europe and Asia. Moreover, we applied Fluorescence in situ Hybridization followed by Catalyzed Reporter Deposition (CARD-FISH) for a first visualization of distinct CPR lineages in freshwater samples. Results A total of 174 dereplicated metagenome-assembled genomes (MAGs) of diverse CPR lineages were recovered from the investigated lakes, with a higher prevalence from hypolimnion samples (162 MAGs). They have reduced genomes (median size 1 Mbp) and were generally found in low abundances (0.02–14.36 coverage/Gb) and with estimated slow replication rates. The analysis of genomic traits and CARD-FISH results showed that the radiation is an eclectic group in terms of metabolic capabilities and potential lifestyles, ranging from what appear to be free-living lineages to host- or particle-associated groups. Although some complexes of the electron transport chain were present in the CPR MAGs, together with ion-pumping rhodopsins and heliorhodopsins, we believe that they most probably adopt a fermentative metabolism. Terminal oxidases might function in O 2 scavenging, while heliorhodopsins could be involved in mitigation against oxidative stress. Conclusions A high diversity of CPR MAGs was recovered, and distinct CPR lineages did not seem to be limited to lakes with specific trophic states. Their reduced metabolic capacities resemble the ones described for genomes in groundwater and animal-associated samples, apart from Gracilibacteria that possesses more complete metabolic pathways. Even though this radiation is mostly host-associated, we also observed organisms from different clades (ABY1, Paceibacteria, Saccharimonadia) that appear to be unattached to any other organisms or were associated with ‘lake snow’ particles (ABY1, Gracilibacteria), suggesting a broad range of potential life-strategies in this phylum. 

/pdf/ecogenomics-sheds-light-on-diverse-lifestyle-strategies-in-1gz1pxnf.pdf

Ecogenomics sheds light on diverse lifestyle strategies in freshwater CPR

Abstract Carbon fixation is a critical process for our planet; however, its distribution across the bacterial and archaeal domains of life has not been comprehensively studied. Here, we performed an analysis of 52,515 metagenome-assembled genomes and discover carbon fixation pathways in 1,007 bacteria and archaea. We reveal the genomic potential for carbon fixation through the reverse tricarboxylic acid cycle in previously unrecognized archaeal and bacterial phyla (i.e. Thermoplasmatota and Elusimicrobiota) and show that the 3-hydroxypropionate bi-cycle is not, as previously thought, restricted to the phylum Chloroflexota. The data also substantially expand the phylogenetic breadth for autotrophy through the dicarboxylate/4-hydroxybutyrate cycle and the Calvin–Benson–Bassham cycle. Finally, the genomic potential for carbon fixation through the 3-hydroxypropionate/4-hydroxybutyrate cycle, previously exclusively found in Archaea, was also detected in the Bacteria. Carbon fixation thus appears to be much more widespread than previously known, and this study lays the foundation to better understand the role of archaea and bacteria in global primary production and how they contribute to microbial carbon sinks.

https://academic.oup.com/pnasnexus/advance-article-pdf/doi/10.1093/pnasnexus/pgac226/46342141/pgac226.pdf

Carbon fixation pathways across the bacterial and archaeal tree of life

Gram-positive bacteria (e.g. Firmicutes) and their mobile genetic elements (plasmids, bacteriophages) encode peptide-based quorum sensing systems (QSSs) that regulate behavioral transitions in a density-dependent manner. In their simplest form, termed “RRNPP”, these QSSs are composed of two adjacent genes: a communication propeptide and its cognate intracellular receptor. Despite the prime importance of RRNPP QSSs in the regulation of key biological pathways such as virulence, sporulation or biofilm formation in bacteria, conjugation in plasmids or lysogeny in temperate bacteriophages, no tools exist to predict their presence in target genomes/mobilomes. Here, we introduce RRNPP_detector, a software to predict RRNPP QSSs in chromosomes, plasmids and bacteriophages of gram-positive bacteria, available at https://github.com/TeamAIRE/RRNPP_detector. RRNPP_detector does not rely on homology searches but on a signature of multiple criteria, which are common between distinct families of experimentally-validated RRNPP QSSs. Because this signature is generic while specific to the canonical mechanism of RRNPP quorum sensing, it enables the discovery of novel RRNPP QSSs and thus of novel “languages” of biocommunication. Applying RRNPP_detector against complete genomes of viruses and Firmicutes available on the NCBI, we report a potential 7.5-fold expansion of RRNPP QSS diversity, alternative secretion-modes for certain candidate QSS propeptides, ‘bilingual’ bacteriophages and plasmids, as well as predicted chromosomal and plasmidic Biosynthetic-Gene-Clusters regulated by QSSs.

/pdf/rrnpp-detector-a-tool-to-detect-rrnpp-quorum-sensing-systems-59hpfmu48h.pdf

RRNPP_detector: a tool to detect RRNPP quorum sensing systems in chromosomes, plasmids and phages of gram-positive bacteria

https://hal.archives-ouvertes.fr/hal-03341509/document

Retracing lineage history: time to emphasize genetic turnover.

Communication between viruses supported by quorum sensing systems (QSSs) were found to optimize the fitness of temperate bacteriophages of Bacilli by guiding the transition from the host-destructive lytic cycle to the host-protective lysogenic cycle in a density-dependent manner. All known phage-encoded QSSs consist of a communication propeptide and a cognate intracellular receptor that regulates the expression of adjacent target genes upon recognition of the matured peptide, a signature known as RRNPP and found in chromosomes, plasmids and phages of Firmicutes bacteria. Recently, we have introduced the RRNPP_detector software to detect novel genetic systems matching the RRNPP signature, which unearthed many novel phage-encoded candidate QSSs. Here, by looking at the adjacent genes likely regulated by these viral candidate QSSs, we identified an unsuspected clustering of viral QSSs with viral genes whose bacterial homologs are key regulators of the last-resort bacterial sporulation initiation pathway (rap, spo0E or abrB). Consistently, we found evidence in published data that certain of these QSSs encoded by prophages (phage genomes inserted within a bacterial genome) dynamically manipulate the timing of sporulation in the host. Because these viral QSSs are genetically diverse and are found associated with different sporulation regulators, this suggests a convergent evolution in bacteriophages of density-dependent sporulation-hijacking mechanisms.

https://www.biorxiv.org/content/biorxiv/early/2021/10/18/2021.07.15.452460.full.pdf

Large-scale identification of viral quorum sensing systems reveals density-dependent sporulation-hijacking mechanisms in bacteriophages

Quorum sensing systems (QSSs) are genetic systems supporting cell-cell or bacteriophage-bacteriophage communication. By regulating behavioral switches as a function of the encoding population density, QSSs shape the social dynamics of microbial communities. However, their diversity is tremendously overlooked in bacteriophages, which implies that many density-dependent behaviors likely remains to be discovered in these viruses. Here, we developed a signature-based computational method to identify novel peptide-based RRNPP QSSs in gram-positive bacteria (e.g. Firmicutes) and their mobile genetic elements. The large-scale application of this method against available genomes of Firmicutes and bacteriophages revealed 2708 candidate RRNPP-type QSSs, including 382 found in (pro)phages. These 382 viral candidate QSSs are classified into 25 different groups of homologs, of which 22 were never described before in bacteriophages. Remarkably, genomic context analyses suggest that candidate viral QSSs from 6 different families dynamically manipulate the host biology. Specifically, many viral candidate QSSs are predicted to regulate, in a density-dependent manner, adjacent (pro)phage-encoded regulator genes whose bacterial homologs are key regulators of the sporulation initiation pathway (either Rap, Spo0E, or AbrB). Consistently, we found evidence from public data that certain of our candidate (pro)phage-encoded QSSs dynamically manipulate the timing of sporulation of the bacterial host. These findings challenge the current paradigm assuming that bacteria decide to sporulate in adverse situation. Indeed, our survey highlights that bacteriophages have evolved, multiple times, genetic systems that dynamically influence this decision to their advantage, making sporulation a survival mechanism of last resort for phage-host collectives.

/pdf/large-scale-identification-of-viral-quorum-sensing-systems-3y36mi9q4o.pdf

Large-scale identification of viral quorum sensing systems reveal convergent evolution of density-dependent sporulation-hijacking in bacteriophages

Autotrophic carbon fixation is a crucial process for sustaining life on Earth. To date, six pathways, the Calvin-Benson-Bassham cycle, the reductive tricarboxylic acid cycle, the 3-hydroxypropionate bi-cycle, the Wood-Ljungdahl pathway, the dicarboxylate/4-hydroxybutyrate cycle, and the 4-hydroxybutyrate cycle have been described. Nanoorganisms, such as members of the Candidate Phyla Radiation (CPR) bacterial superphylum and the Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohalorchaeota (DPANN) archaeal superphylum, could deeply impact carbon cycling and carbon fixation in ways that are still to be determined. CPR and DPANN are ubiquitous in the environment but understudied; their gene contents are not exhaustively described, and their metabolisms are not yet fully understood. Here, the completeness of each of the above pathways were quantified and tested for the presence of all key enzymes in a diversity of nanoorganisms across the World Ocean. The novel marine ultra-small prokaryotes was demonstrated to collectively harbor the genes required for carbon fixation, in particular the ‘energetically efficient’ DH pathway, and HBC pathways. This contrasted with the known carbon metabolic pathways associated with CPR memebers in aquifers, where they are described as degraders (Castelle 2015 et al., 2015, Castelle et al., 2018, Anantharaman et al., 2016). Our findings offer the possibility that nanoorganisms have a broader contribution to carbon fixation and cycling than currently assumed. Furthermore, CPR and DPANN are possibly not the only nanosized prokaryotes; therefore, the discovery of new autotrophic marine nanoorganisms, by future single cell genomics is anticipated.

/pdf/carbon-fixation-by-marine-ultrasmall-prokaryotes-1tll2f7c50.pdf

Carbon Fixation by Marine Ultrasmall Prokaryotes.

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