The Dynamic Nature of Genomes Across the Tree of Life

Genomes are dynamic in lineages across the tree of life. Among bacteria and archaea, for example, DNA content varies through out life cycles, and nonbinary cell division in diverse lineages indicates the need for coordination of the inheritance of genomes. These observations contrast with the textbook view that bacterial and archaeal genomes are monoploid (i.e., single copied) and fixed both within species and throughout an individual\u27s lifetime. Here, we synthesize information on three aspects of dynamic genomes from exemplars representing a diverse array of bacterial and archaeal lineages: 1) ploidy level variation, 2) epigenetic mechanisms, and 3) life cycle variation. For example, the Euryarchaeota analyzed to date are all polyploid, as is the bacterium Epulopiscium that contains up to tens of thousands of copies of its genome and reproduces by viviparity. The bacterium Deinococcus radiodurans and the archaeon Halobacterium sp. NRC-1 can repair a highly fragmented genome within a few hours. Moreover, bacterial genera such as Dermocarpella and Planctomyces reproduce by fission (i.e., generating many cells from one cell) and budding, respectively, highlighting the need for regulation of genome inheritance in these lineages. Combining these data with our previous work on widespread genome dynamics among eukaryotes, we hypothesize that dynamic genomes are a rule rather than the exception across the tree of life. Further, we speculate that all domains may have the ability to distinguish germline from somatic DNA and that this ability may have been present the last universal common ancestor

Are Microbes Fundamentally Different Than Macroorganisms? Convergence and a Possible Case for Neutral Phenotypic Evolution in Testate Amoeba (Amoebozoa: Arcellinida)

This study reveals extensive phenotypic convergence based on the non-monophyly of genera and morphospecies of testate (shelled) amoebae. Using two independent markers, small subunit ribosomal DNA (ssu-rDNA) and mitochondrial cytochrome oxidase I (COI), we demonstrate discordance between morphology and molecules for ‘core Nebela’ species (Arcellinida; Amoebozoa). Prior work using just a single locus, ssu-rDNA, also supported the non-monophyly of the genera Hyalosphenia and Nebela as well as for several morphospecies within these genera. Here, we obtained COI gene sequences of 59 specimens from seven morphospecies and ssu-rDNA gene sequences of 50 specimens from six morphospecies of hyalosphenids. Our analyses corroborate the prior ssu-rDNA findings of morphological convergence in test (shell) morphologies, as COI and ssu-rDNA phylogenies are concordant. Further, the monophyly of morphospecies is rejected using approximately unbiased tests. Given that testate amoebae are used as bioindicators in both palaeoecological and contemporary studies of threatened ecosystems such as bogs and fens, understanding the discordance between morphology and genetics in the hyalosphenids is essential for interpretation of indicator species. Further, while convergence is normally considered the result of natural selection, it is possible that neutrality underlies phenotypic evolution in these microorganisms

The Role of Phosphorus Limitation in Shaping Soil Bacterial Communities and Their Metabolic Capabilities.

Phosphorus (P) is an essential nutrient that is often in limited supply, with P availability constraining biomass production in many terrestrial ecosystems. Despite decades of work on plant responses to P deficiency and the importance of soil microbes to terrestrial ecosystem processes, how soil microbes respond to, and cope with, P deficiencies remains poorly understood. We studied 583 soils from two independent sample sets that each span broad natural gradients in extractable soil P and collectively represent diverse biomes, including tropical forests, temperate grasslands, and arid shrublands. We paired marker gene and shotgun metagenomic analyses to determine how soil bacterial and archaeal communities respond to differences in soil P availability and to detect corresponding shifts in functional attributes. We identified microbial taxa that are consistently responsive to extractable soil P, with those taxa found in low P soils being more likely to have traits typical of oligotrophic life history strategies. Using environmental niche modeling of genes and gene pathways, we found an enriched abundance of key genes in low P soils linked to the carbon-phosphorus (C-P) lyase and phosphonotase degradation pathways, along with key components of the high-affinity phosphate-specific transporter (Pst) and phosphate regulon (Pho) systems. Taken together, these analyses suggest that catabolism of phosphonates is an important strategy used by bacteria to scavenge phosphate in P-limited soils. Surprisingly, these same pathways are important for bacterial growth in P-limited marine waters, highlighting the shared metabolic strategies used by both terrestrial and marine microbes to cope with P limitation.</div

A global atlas of the dominant bacteria found in soil.

A global atlas of the dominant bacteria found in soil. Published in Science. http://science.sciencemag.org/content/359/6373/32

Spatial and temporal metagenomics of river compartments reveals viral community dynamics in an urban impacted stream

Although river ecosystems constitute a small fraction of Earth’s total area, they are critical modulators of microbially and virally orchestrated global biogeochemical cycles. However, most studies either use data that is not spatially resolved or is collected at timepoints that do not reflect the short life cycles of microorganisms. To address this gap, we assessed how viral and microbial communities change over a 48-hour period by sampling surface water and pore water compartments of the wastewater-impacted River Erpe in Germany. We sampled every 3 hours resulting in 32 samples for which we obtained metagenomes along with geochemical and metabolite measurements. From our metagenomes, we identified 6,500 viral and 1,033 microbial metagenome assembled genomes (MAGs) and found distinct community membership and abundance associated with each river compartment (e.g., Competibacteraceae in surfacewater and Sulfurimonadaceae in pore water). We show that 17% of our viral MAGs clustered to viruses from other ecosystems like wastewater treatment plants and rivers. Our results also indicated that 70% of the viral community was persistent in surface waters, whereas only 13% were persistent in the pore waters taken from the hyporheic zone. Finally, we predicted linkages between 73 viral genomes and 38 microbial genomes. These putatively linked hosts included members of the Competibacteraceae, which we suggest are potential contributors to river carbon and nitrogen cycling via denitrification and nitrogen fixation. Together, these findings demonstrate that members of the surface water microbiome from this urban river are stable over multiple diurnal cycles. These temporal insights raise important considerations for ecosystem models attempting to constrain dynamics of river biogeochemical cycles

Transglutaminase 2 Contributes to Apoptosis Induction in Jurkat T Cells by Modulating Ca(2+) Homeostasis via Cross-Linking RAP1GDS1

BACKGROUND: Transglutaminase 2 (TG2) is a protein cross-linking enzyme known to be associated with the in vivo apoptosis program of T cells. However, its role in the T cell apoptosis program was not investigated yet. RESULTS: Here we report that timed overexpression of both the wild type (wt) and the cross-linking mutant of TG2 induced apoptosis in Jurkat T cells, the wt being more effective. Part of TG2 colocalised with mitochondria. WtTG2-induced apoptosis was characterized by enhanced mitochondrial Ca(2+) uptake. Ca(2+)-activated wtTG2 cross-linked RAP1, GTP-GDP dissociation stimulator 1, an unusual guanine exchange factor acting on various small GTPases, to induce a yet uncharacterized signaling pathway that was able to promote the Ca(2+) release from the endoplasmic reticulum via both Ins3P and ryanodine sensitive receptors leading to a consequently enhanced mitochondrial Ca(2+)uptake. CONCLUSIONS: Our data indicate that TG2 might act as a Ca(2+) sensor to amplify endoplasmic reticulum-derived Ca(2+) signals to enhance mitochondria Ca(2+) uptake. Since enhanced mitochondrial Ca(2+) levels were previously shown to sensitize mitochondria for various apoptotic signals, our data demonstrate a novel mechanism through which TG2 can contribute to the induction of apoptosis in certain cell types. Since, as compared to knock out cells, physiological levels of TG2 affected Ca(2+) signals in mouse embryonic fibroblasts similar to Jurkat cells, our data might indicate a more general role of TG2 in the regulation of mitochondrial Ca(2+) homeostasis

Extreme environments offer an unprecedented opportunity to understand microbial eukaryotic ecology, evolution, and genome biology

Abstract Research in extreme environments has substantially expanded our understanding of the ecology and evolution of life on Earth, but a major group of organisms has been largely overlooked: microbial eukaryotes (i.e., protists). In this Perspective, we summarize data from over 80 studies of protists in extreme environments and identify focal lineages that are of significant interest for further study, including clades within Echinamoebida, Heterolobosea, Radiolaria, Haptophyta, Oomycota, and Cryptophyta. We argue that extreme environments are prime sampling targets to fill gaps in the eukaryotic tree of life and to increase our understanding of the ecology, metabolism, genome architecture, and evolution of eukaryotic life

The global-scale distributions of soil protists and their contributions to belowground systems

Protists are ubiquitous in soil, where they are key contributors to nutrient cycling and energy transfer. However, protists have received far less attention than other components of the soil microbiome. We used amplicon sequencing of soils from 180 locations across six continents to investigate the ecological preferences of protists and their functional contributions to belowground systems. We complemented these analyses with shotgun metagenomic sequencing of 46 soils to validate the identities of the more abundant protist lineages. We found that most soils are dominated by consumers, although parasites and phototrophs are particularly abundant in tropical and arid ecosystems, respectively. The best predictors of protist composition (primarily annual precipitation) are fundamentally distinct from those shaping bacterial and archaeal communities (namely, soil pH). Some protists and bacteria co-occur globally, highlighting the potential importance of these largely undescribed belowground interactions. Together, this study allowed us to identify the most abundant and ubiquitous protists living in soil, with our work providing a cross-ecosystem perspective on the factors structuring soil protist communities and their likely contributions to soil functioning.A.M.O. acknowledges support from the NSF Graduate Research Fellowship and the CIRES Graduate Fellowship. S.G. acknowledges support from the NWO-VENI grant from the Netherlands Organisation for Scientific Research (016.Veni.181.078). M.D.-B. acknowledges the support from the Marie Skłodowska-Curie Actions of the Horizon 2020 Framework Programme H2020-MSCA-IF-2016 under REA grant agreement no. 702057 (CLIMIFUN). F.T.M. acknowledges support from European Research Council grant agreement no. 647038 (BIODESERT). Support to N.F. was provided by the Simons Foundation, the Smithsonian Tropical Research Institute, and the U.S. NSF (DEB 1556090)

How Discordant Morphological and Molecular Evolution Among Microorganisms Can Revise our Notions of Biodiversity on Earth

Microscopy has revealed tremendous diversity of bacterial and eukaryotic forms. Recent molecular analyses show discordance in estimates of biodiversity between morphological and molecular analyses. Moreover, phylogenetic analyses of the diversity of microbial forms reveal evidence of convergence at scales as deep as interdomain: morphologies shared between bacteria and eukaryotes. Here, we highlight examples of such discordance, focusing on exemplary lineages such as testate amoebae, ciliates, and cyanobacteria. These have long histories of morphological study, enabling deeper analyses on both the molecular and morphological sides. We discuss examples in two main categories: (i) morphologically identical (or highly similar) individuals that are genetically distinct and (ii) morphologically distinct individuals that are genetically the same. We argue that hypotheses about discordance can be tested using the concept of neutral morphologies, or more broadly neutral phenotypes, as a null hypothesis