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bioRxiv2017

Hydrogen production by Sulfurospirillum spp. enables syntrophic interactions of Epsilonproteobacteria

Hydrogen-producing bacteria are of environmental and biotechnological importance in anoxic environments, since hydrogen is an important electron donor for prokaryotes and of interest as an alternative energy source. Epsilonproteobacteria, inhabiting ecologically, clinically or biotechnologically relevant environments, are currently considered to be hydrogen-oxidizing bacteria exclusively. Here, we report hydrogen production for a genus of free-living Epsilonproteobacteria, Sulfurospirillum spp. inhabiting sediments, wastewater plants, bioelectrodes, oil reservoirs, contaminated areas, or marine habitats. The amount of hydrogen production was largely different in two subgroups of Sulfurospirillum spp., represented by S. cavolei and S. multivorans. The former is shown to be the more potent hydrogen producer and excretes acetate as sole organic acid, while the latter exhibited a more flexible fermentation, producing additionally lactate and succinate. The observed hydrogen production could be assigned to a group 4 hydrogenase similar to Hydrogenase 4 (Hyf) in E. coli. We propose that Sulfurospirillum spp. produce molecular hydrogen with electrons derived from pyruvate oxidation by pyruvate:ferredoxin oxidoreductase and reduced ferredoxin. This hypothesis is supported by comparative proteome data, in which both PFOR and ferredoxin as well as hydrogenase 4 are up-regulated. A co-culture experiment with S. multivorans and Methanococcus voltae cultivated with lactate as sole substrate shows a syntrophic interaction between both organisms, since the former cannot grow fermentatively on lactate alone and the latter relies on hydrogen as electron donor. This opens up new perspectives on microbial communities, since Epsilonproteobacteria could play a yet unrecognized role as hydrogen producers in anoxic microbial communities.

microbiology↗

bioRxiv2017

Hematology, biochemistry, and toxicology of wild hawksbill turtles (Eretmochelys imbricata) nesting in mangrove estuaries in the eastern Pacific Ocean

Sea turtles are a keystone species and are highly sensitive to changes in their environment, making them excellent environmental indicators. In light of environmental and climate changes, species are increasingly threatened by pollution, changes in ocean health, habitat alteration, and plastic ingestion. There may be additional health related threats and understanding these threats is key in directing future management and conservation efforts, particularly for severely reduced sea turtle populations. Hawksbill turtles (Eretmochelys imbricata) are critically endangered, with those in the eastern Pacific Ocean (Mexico-Peru) considered one of the most threatened sea turtle populations in the world. This study establishes baseline health parameters in hematology and blood biochemistry as well as tested for heavy metals and persitent organic pollutants in eastern Pacific hawksbills at a primary nesting colony located in a mangrove estuary. Whereas hematology and biochemistry results are consistent with healthy populations of other species of sea turtles, we identified differences in packed cell volume, heterophils and lympohcyte counts, and glucose when comparing our data to other adult hawksbill analysis (1), (2), (3). Our analysis of heavy metal contamination revealed a mean blood level of 0.245 ppm of arsenic, 0.045 ppm of lead, and 0.008 ppm of mercury. Blood levels of persistent organic pollutants were below the laboratory detection limit for all turtles. Our results suggest that differences in the feeding ecology of eastern Pacific hawksbills in mangrove estuaries may make them less likely to accumulate persistent organic pollutants and heavy metals in their blood. These baseline data on blood values in hawksbills nesting within a mangrove estuary in the eastern Pacific offer important guidance for health assessments of the species in the wild and in clinical rehabilitation facilities, and underscore the importance of preventing contamination from point and non-point sources in mangrove estuaries, which represent primary habitat to hawksbills and myriad other marine species in the eastern Pacific Ocean.

zoology↗

bioRxiv2017

The null additivity of multi-drug combinations

From natural ecology 1-4 to clinical therapy 5-8, cells are often exposed to mixtures of multiple drugs. Two competing null models are used to predict the combined effect of drugs: response additivity (Bliss) and dosage additivity (Loewe) 9-11. Here, noting that these models diverge with increased number of drugs, we contrast their predictions with measurements of Escherichia coli growth under combinations of up to 10 different antibiotics. As the number of drugs increases, Bliss maintains accuracy while Loewe systematically loses its predictive power. The total dosage required for growth inhibition, which Loewe predicts should be fixed, steadily increases with the number of drugs, following a square root scaling. This scaling is explained by an approximation to Bliss where, inspired by RA Fishers classical geometric model 12, dosages of independent drugs adds up as orthogonal vectors rather than linearly. This dose-orthogonality approximation provides results similar to Bliss, yet uses the dosage language as Loewe and is hence easier to implement and intuit. The rejection of dosage additivity in favor of effect additivity and dosage orthogonality provides a framework for understanding how multiple drugs and stressors add up in nature and the clinic.

systems biology↗

bioRxiv2017

Sex-determination and sex chromosomes are shared across the radiation of dioecious Nepenthes pitcher plants

Plants with separate sexes (dioecy) represent a minority but dioecy has evolved multiple times independently in plants. Our understanding of sex determination systems in plants and of the ecological factors and molecular changes associated with the evolution of dioecy remain limited. Here, we study the sex-determination system in dioecious plants that lack heteromorphic sex chromosomes and are not amenable to controlled breeding: Nepenthes pitcher plants. We genotyped wild populations of flowering males and females of three Nepenthes taxa using ddRAD-seq, and sequenced a male inflorescence transcriptome. We developed a novel statistical tool (privacy rarefaction) to distinguish true sex-specificity from stochastic noise in high-throughput sequencing data. Our results support XY-systems in all three Nepenthes taxa and in Silene latifolia which was used as a positive control for its known XY-system. The male-specific region of the Y chromosome showed little conservation among the three Nepenthes taxa, except for the essential pollen development gene DYT1 which was also male-specific in additional taxa. Hence, this homomorphic XY sex-determination system likely has a unique origin older than the crown of the genus Nepenthes at c. 17.7 My. In addition to the characterisation of the previously unknown sex chromosomes of Nepenthes, our work contributes an innovative, highly sensitive statistical method to efficiently detect sex-specific genomic regions in wild populations in general.

evolutionary biology↗

bioRxiv2017

Decoding the gene co-expression network underlying the ability of Gevuina avellana Mol. to live in diverse light conditions

O_LIGevuina avellana Mol. (Proteaceae) is a typical tree from the South American temperate rainforest. Although this species mostly regenerates in shaded understories, it exhibits an exceptional ecological breadth, being able to live under a wide range of light conditions. Here we studied the genetic basis regulating physiological acclimation of the photosynthetic responses of G. avellana under contrasting light conditions.\nC_LIO_LIWe analyzed carbon assimilation and light energy used for photochemical process in plants acclimated to contrasting light conditions. Also, we used a transcriptional profile of leaf primordia from G. avellana saplings growing under different light environments to identify the gene co-expression network underpinning photosynthetic performance and light-related processes.\nC_LIO_LIThe photosynthetic parameters revealed optimal performance regardless of light conditions. Strikingly, the mechanism involved in dissipation of excess light energy showed no significant differences between high and low-light acclimated plants. The gene co-expression network defined a community structure consistent with the photochemical responses, including genes involved mainly in assembly and functioning of photosystems, photoprotection, and retrograde signaling.\nC_LIO_LIOur ecophysiological genomics approach provides an understanding of the molecular regulatory mechanisms that allows this tree to have an optimal balance between photochemical, photoprotective and antioxidant performance in the diverse light habitats it encounters in nature.\nC_LI

plant biology↗

bioRxiv2017

Proposal for practical multi-kingdom classification of eukaryotes based on monophyly and comparable divergence time criteria

Much of the ecological, taxonomic and biodiversity research relies on understanding of phylogenetic relationships among organisms. There are multiple available classification systems that all suffer from differences in naming, incompleteness, presence of multiple non-monophyletic entities and poor correspondence of divergence times. These issues render taxonomic comparisons across the main groups of eukaryotes and all life in general difficult at best. By using the monophyly criterion, roughly comparable time of divergence and information from multiple phylogenetic reconstructions, I propose an alternative classification system for the domain Eukarya to improve hierarchical taxonomical comparability for animals, plants, fungi and multiple protist groups. Following this rationale, I propose 32 kingdoms of eukaryotes that are treated in 10 subdomains. These kingdoms are further separated into 43, 115, 140 and 353 taxa at the level of subkingdom, phylum, subphylum and class, respectively (http://dx.doi.org/10.15156/BIO/587483). Most of the names have been used previously or these were deduced from those of the type taxa to be able to unambiguously link genera to higher taxonomic levels. In the era of phylogenomics, understanding about the phylogenetic relationships among organisms is rapidly increasing. Classifications systems must keep pace with this race to serve the research community by consistent improvements in precision in terms of taxonomic resolution and maintaining monophyly of the ingredient taxa.

evolutionary biology↗

bioRxiv2017

Genome-wide association across Saccharomyces cerevisiae strains reveals substantial variation in underlying gene requirements for toxin tolerance.

Cellulosic plant biomass is a promising sustainable resource for generating alternative biofuels and biochemicals with microbial factories. But a remaining bottleneck is engineering microbes that are tolerant of toxins generated during biomass processing, because mechanisms of toxin defense are only beginning to emerge. Here, we exploited natural diversity in 165 Saccharomyces cerevisiae strains isolated from diverse geographical and ecological niches, to identify mechanisms of hydrolysate-toxin tolerance. We performed genome-wide association (GWA) analysis to identify genetic variants underlying toxin tolerance, and gene knockouts and allele-swap experiments to validate the involvement of implicated genes. In the process of this work, we uncovered a surprising difference in genetic architecture depending on strain background: in all but one case, knockout of implicated genes had a significant effect on toxin tolerance in one strain, but no significant effect in another strain. In fact, whether or not the gene was involved in tolerance in each strain background had a bigger contribution to strain-specific variation than allelic differences. Our results suggest a major difference in the underlying network of causal genes in different strains, suggesting that mechanisms of hydrolysate tolerance are very dependent on the genetic background. These results could have significant implications for interpreting GWA results and raise important considerations for engineering strategies for industrial strain improvement.\n\nAuthor summaryUnderstanding the genetic architecture of complex traits is important for elucidating the genotype-phenotype relationship. Many studies have sought genetic variants that underlie phenotypic variation across individuals, both to implicate causal variants and to inform on architecture. Here we used genome-wide association analysis to identify genes and processes involved in tolerance of toxins found in plant-biomass hydrolysate, an important substrate for sustainable biofuel production. We found substantial variation in whether or not individual genes were important for tolerance across genetic backgrounds. Whether or not a gene was important in a given strain background explained more variation than the alleleic differences in the gene. These results suggest substantial variation in gene contributions, and perhaps underlying mechanisms, of toxin tolerance.

genomics↗

bioRxiv2018

High-magnitude innovators as keystone individuals in the evolution of culture

Borrowing from the concept of keystone species in ecological food webs, a recent focus in the field of animal behaviour has been keystone individuals: individuals whose impact on population dynamics is disproportionally larger than their frequency in the population. In populations evolving culture, such may be the role of high-magnitude innovators: individuals whose innovations are a major departure from the populations existing behavioural repertoire. Their effect on cultural evolution is twofold: they produce innovations that constitute a cultural leap, and, once copied, their innovations may induce further innovations by conspecifics (socially induced innovations), as they explore the new behaviour themselves. I use computer simulations to study the co-evolution of independent innovations, socially induced innovations, and innovation magnitude, and show that while socially induced innovation is assumed here to be less costly than independent innovation, it does not readily evolve. When it evolves, it may in some conditions select against independent innovation and lower its frequency, despite it requiring independent innovation in order to operate; at the same time, however, it leads to much faster cultural evolution. These results confirm the role of high-magnitude innovators as keystones, and suggest a novel explanation for low frequency of independent innovation.

animal behavior and cognition↗

bioRxiv2018

The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water

The semi-aquatic bugs conquered water surfaces worldwide and occupy ponds, streams, lakes, mangroves, and even open oceans. As such, they inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders thorough investigations of the mechanisms underlying the processes of adaptation and diversification in this group. Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome, the first water strider genome to be sequenced so far. G. buenoi genome is about 1 000Mb and the sequencing effort recovered 20 949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to water surface lifestyle. These expansions affect key processes such as growth, vision, desiccation resistance, detoxification, olfaction and epigenetic components. Strikingly, the G. buenoi genome contains three Insulin Receptors, a unique case among metazoans, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes include wavelength sensitivity shifts in opsin proteins likely in association with the requirements of vision in water habitats. Our findings suggest that local gene duplications might have had an important role during the evolution of water striders. These findings along with the G. buenoi genome open exciting research opportunities to understand adaptation and genome evolution of this unique hemimetabolous insect.

genomics↗

bioRxiv2018

Pyrimidine starvation activates a bistable phenotypic switch leading to ribosome provisioning and rapid exit from stationary phase

Observations of bacteria at the single-cell level have revealed many instances of phenotypic heterogeneity within otherwise clonal populations, but the selective causes, molecular bases and broader ecological relevance remain poorly understood. In an earlier experiment in which the bacterium Pseudomonas fluorescens SBW25 was propagated under a selective regime that mimicked the host immune response, a genotype evolved that stochastically switched between capsulation states. The genetic cause was a mutation in carB that decreased the pyrimidine pool (and growth rate), lowering the activation threshold of a pre-existing but hitherto unrecognised phenotypic switch. Genetic components surrounding bifurcation of UTP flux towards DNA/RNA or UDP-glucose (a precursor of colanic acid forming the capsules) were implicated as key components. Extending these molecular analyses - and based on a combination of genetics, transcriptomics, biochemistry and mathematical modelling - we show that pyrimidine limitation triggers an increase in ribosome biosynthesis and that switching is caused by competition between ribosomes and CsrA/RsmA proteins for the mRNA transcript of a feed-forward regulator of colanic acid biosynthesis. We additionally show that in the ancestral bacterium the switch is part of a programme that determines stochastic entry into the semi-quiescent capsulated state, ensures that such cells are provisioned with excess ribosomes, and enables provisioned cells to exit rapidly from stationary phase under permissive conditions.

microbiology↗

bioRxiv2018

Genome-wide scans of selection highlight the impact of biotic and abiotic constraints in natural populations of the model grass Brachypodium distachyon.

Grasses are essential plants for ecosystem functioning. Quantifying the selective pressures that act on natural variation in grass species is therefore essential regarding biodiversity maintenance. In this study, we investigate the selection pressures that act on two distinct populations of the grass model Brachypodium distachyon without prior knowledge about the traits under selection. We took advantage of whole-genome sequencing data produced for 44 natural accessions of B. distachyon and used complementary genome-wide scans of selection (GWSS) methods to detect genomic regions under balancing and positive selection. We show that selection is shaping genetic diversity at multiple temporal and spatial scales in this species and affects different genomic regions across the two populations. Gene Ontology annotation of candidate genes reveals that pathogens may constitute important factors of positive and balancing selection in Brachypodium distachyon. We eventually cross-validated our results with QTL data available for leaf-rust resistance in this species and demonstrate that, when paired with classical trait mapping, GWSS can help pinpointing candidate genes for further molecular validation. Thanks to a near-base perfect reference genome and the large collection of freely available natural accessions collected across its natural range, B. distachyon appears as a prime system for studies in ecology, population genomics and evolutionary biology.

evolutionary biology↗

bioRxiv2018

Microbial biogeography of 1,000 geothermal springs in New Zealand

Geothermal springs are model ecosystems to systematically investigate microbial biogeography as they i) represent discrete, homogenous habitats; ii) are abundantly distributed across multiple geographical scales; iii) span broad geochemical gradients; and iv) have simple community structures with reduced metazoan interactions. Taking advantage of these traits, we undertook the largest known consolidated study of geothermal ecosystems (http://1000springs.org.nz) to determine factors that influence biogeographical patterns. Rigorously standardised methodologies were used to measure microbial communities, 46 physicochemical parameters, and metadata from 1,019 hotspring samples across New Zealand. pH was found to be the primary influence on diversity in springs < 70 {degrees}C with community similarity decreasing with geographic distance. Surprisingly, community composition was dominated by two genera (Venenivibrio and Acidithiobacillus) in both average relative abundance (11.2 and 11.1 %) and prevalence (74.2 and 62.9 % respectively) across physicochemical spectrums of 13.9 - 100.6 {degrees}C and pH < 1 - 9.7. This study provides an unprecedented insight into the ecological conditions that drive community assembly in geothermal springs, and can be used as a foundation to improve the characterisation of global microbial biogeographical processes.

microbiology↗

bioRxiv2018

An evolutionary innovation is contingent on maintaining adaptive potential until competition subsides

After 15 years of the Lenski experiment one of twelve Escherichia coli populations evolved the ability to utilize an abundant but previously untapped carbon source, citrate. Mutations responsible for the appearance of rudimentary citrate utilization (Cit+ phenotype) and for refining this ability have been characterized. However, the complete nature of the genetic and/or ecological events that set the stage for this key innovation remain unknown. We found that there was a slight fitness benefit for introducing an activated citT cassette that mimics the mutation causing Cit+ into the ancestor of the evolution experiment and strains isolated from the population close to when it evolved. However, there was no benefit or even a large deleterious effect in intermediate strains. We conclude that achieving Cit+ was contingent on both an evolutionary trajectory that maintained a potentiated genetic state and the slowing rate of adaptation in this population late in the experiment.

evolutionary biology↗

bioRxiv2018

Extensive genomic diversity among Mycobacterium marinum strains revealed by whole genome sequencing

Mycobacterium marinum is the causative agent for the tuberculosis-like disease mycobacteriosis in fish and skin lesions in humans. Ubiquitous in its geographical distribution, M. marinum is known to occupy diverse fish as hosts. However, information about its genomic diversity is limited. Here, we provide the genome sequences for 15 M. marinum strains isolated from infected humans and fish. Comparative genomic analysis of these and four available genomes of the M. marinum strains M, E11, MB2 and Europe reveal high genomic diversity among the strains, leading to the conclusion that M. marinum should be divided into two different clusters, the \"M\"- and the \"Aronson\"-type. We suggest that these two clusters should be considered, if not two separate species, at least two M. marinum subspecies. Our data also show that the M. marinum pan-genome for both groups is open and expanding and we provide data showing high number of mutational hotspots in M. marinum relative to other mycobacteria such as Mycobacterium tuberculosis. This high genomic diversity might be related to that M. marinum occupy different ecological niches.

genomics↗

bioRxiv2018

The Principle of Similitude in Biology: From Allometry to the Formulation of Dimensionally Homogenous ‘Laws’

Meaningful laws of nature must be independent of the units employed to measure the variables. The principle of similitude (Rayleigh 1915) or dimensional homogeneity, states that only commensurable quantities (ones having the same dimension) may be compared, therefore, meaningful laws of nature must be homogeneous equations in their various units of measurement, a result which was formalized in the {Pi} theorem (Vaschy 1892; Buckingham 1914). However, most relations in allometry do not satisfy this basic requirement, including the 3/4 Law (Kleiber 1932) that relates the basal metabolic rate and body mass, besides it is sometimes claimed to be the most fundamental biological rate (Brown et al. 2004) and the closest to a law in life sciences (Brown et al. 2004). Using the {Pi} theorem, here we show that it is possible to construct an unique homogeneous equation for the metabolic rates, in agreement with data in the literature. We find that the variations in the dependence of the metabolic rates on body mass are secondary, coming from variations in the allometric dependence of the heart frequencies. This includes not only different classes of animals (mammals, birds, invertebrates) but also different aerobic conditions (basal and maximal). Our results demonstrate that most of the differences found in the allometric exponents (White et al. 2007) are due to compare incommensurable quantities and that our dimensionally homogenous formula, unify these differences into a single formulation. We discuss the ecological implications of this new formulation in the context of the Malthusians, Fenchels and Calders relations.

biophysics↗

bioRxiv2018

Parallels between experimental and natural evolution of legume symbionts

The emergence of symbiotic interactions has been studied using population genomics in nature and experimental evolution in the laboratory, but the parallels between these processes remain unknown. We compared the emergence of rhizobia after the horizontal transfer of a symbiotic plasmid in natural populations of Cupriavidus taiwanensis, over 10 MY ago, with the experimental evolution of symbiotic Ralstonia solanacearum for a few hundred generations. In spite of major differences in terms of time-span, environment, genetic background and phenotypic achievement, both processes resulted in rapid diversification dominated by purifying selection concomitant with acquisition of positively selected mutations. The latter were lacking in the plasmid carrying the genes responsible for the ecological transition. Instead, adaptation targeted the same set of genes leading to the cooption of the same quorum-sensing system. Our results provide evidence for similarities in experimental and natural evolutionary transitions and highlight the potential of comparisons between both processes to understand symbiogenesis.

evolutionary biology↗

bioRxiv2018

Genetic Signatures of Lipid Metabolism Evolution in Cetacea

In mammalian evolutionary history, Cetacea (whales, dolphins, and porpoises) achieved astonishing success by adapting to an aquatic environment. One unique characteristic of cetaceans, contributing to this adaptive success, is efficient lipid utilization. Here we report comparative genetic analysis of aquatic and terrestrial Cetartiodactyla using 144 genes associated with lipid metabolism. We analyzed mutation rate, amino acid substitution, and metabolic pathways using genetic data publicly available. Our test detected 18 positively selected genes in Cetacea compared to 13 in Bovidae with little overlap between the lineages. We identified lineage-specific patterns of amino acid substitutions and functional domain that were mutually exclusive between cetaceans and bovids, supporting divergent evolution of lipid metabolism since the divergence of these taxa from a common ancestor. Moreover, a pathway analysis showed that the identified genes in cetaceans were associated with lipid digestion, lipid storage, and energy producing pathways. This study emphasizes the evolutionary context of lipid metabolism modification of cetaceans and provides a foundation for future studies of elucidating the adapted biological mechanisms of cetacean lipid metabolism and a framework for incorporating ecological context into studies aimed at investigating adaptive evolution.

evolutionary biology↗

bioRxiv2018

The neural representation of missing speech and the influence of prior knowledge on cortical fidelity and latency

In naturally noisy listening conditions, for example at a cocktail party, noise disruptions may completely mask significant parts of a sentence, and yet listeners may still perceive the missing speech as being present. Here we demonstrate that dynamic speech-related auditory cortical activity, as measured by magnetoencephalography (MEG), which can ordinarily be used to directly reconstruct to the physical speech stimulus, can also be used to \"reconstruct\" acoustically missing speech. The extent to which this occurs depends on the extent that listeners are familiar with the missing speech, which is consistent with this neural activity being a dynamic representation of perceived speech even if acoustically absence. Our findings are two-fold: first, we find that when the speech is entirely acoustically absent, the acoustically absent speech can still be reconstructed with performance up to 25% of that of acoustically present speech without noise; and second, that this same expertise facilitates faster processing of natural speech by approximately 5 ms. Both effects disappear when listeners have no or very little prior experience with a given sentence. Our results suggest adaptive mechanisms of consolidation of detailed representations about speech, and the enabling of strong expectations this entails, as identifiable factors assisting automatic speech restoration over ecologically relevant timescales.

neuroscience↗