RESUMO
Yeasts are prevalent in the open ocean, yet we have limited understanding of their ecophysiological adaptations, including their response to nitrogen availability, which can have a major role in determining the ecological potential of other planktonic microbes. In this study, we characterized the nitrogen uptake capabilities and growth responses of marine-occurring yeasts. Yeast isolates from the North Atlantic Ocean were screened for growth on diverse nitrogen substrates, and across a concentration gradient of three environmentally relevant nitrogen substrates: nitrate, ammonium, and urea. Three strains grew with enriched nitrate while two did not, demonstrating that nitrate utilization is present but not universal in marine yeasts, consistent with existing knowledge of nonmarine yeast strains. Naganishia diffluens MBA_F0213 modified the key functional trait of cell size in response to nitrogen concentration, suggesting yeast cell morphology changes along chemical gradients in the marine environment. Meta-analysis of the reference DNA barcode in public databases revealed that the genus Naganishia has a global ocean distribution, strengthening the environmental applicability of the culture-based observations. This study provides novel quantitative understanding of the ecophysiological and morphological responses of marine-derived yeasts to variable nitrogen availability in vitro, providing insight into the functional ecology of yeasts within pelagic open ocean environments.
Assuntos
Nitratos , Nitrogênio , Água do Mar , Nitrogênio/metabolismo , Água do Mar/microbiologia , Nitratos/metabolismo , Oceano Atlântico , Leveduras/metabolismo , Leveduras/genética , Leveduras/crescimento & desenvolvimento , Compostos de Amônio/metabolismo , Ureia/metabolismoRESUMO
Lichens are exemplar symbioses based upon carbon exchange between photobionts and their mycobiont hosts. Historically considered a two-way relationship, some lichen symbioses have been shown to contain multiple photobiont partners; however, the way in which these photobiont communities react to environmental change is poorly understood. Lichina pygmaea is a marine cyanolichen that inhabits rocky seashores where it is submerged in seawater during every tidal cycle. Recent work has indicated that L. pygmaea has a complex photobiont community including the cyanobionts Rivularia and Pleurocapsa. We performed rRNA-based metabarcoding and mRNA metatranscriptomics of the L. pygmaea holobiont at high and low tide to investigate community response to immersion in seawater. Carbon exchange in L. pygmaea is a dynamic process, influenced by both tidal cycle and the biology of the individual symbiotic components. The mycobiont and two cyanobiont partners exhibit distinct transcriptional responses to seawater hydration. Sugar-based compatible solutes produced by Rivularia and Pleurocapsa in response to seawater are a potential source of carbon to the mycobiont. We propose that extracellular processing of photobiont-derived polysaccharides is a fundamental step in carbon acquisition by L. pygmaea and is analogous to uptake of plant-derived carbon in ectomycorrhizal symbioses.
Assuntos
Ascomicetos , Cianobactérias , Líquens , Ascomicetos/fisiologia , Líquens/genética , Cianobactérias/genética , Simbiose , FilogeniaRESUMO
Diatoms are globally abundant microalgae that form extensive blooms in aquatic ecosystems. Certain bacteria behave antagonistically towards diatoms, killing or inhibiting their growth. Despite their crucial implications to diatom blooms and population health, knowledge of diatom antagonists in the environment is fundamentally lacking. We report systematic characterisation of the diversity and seasonal dynamics of bacterial antagonists of diatoms via plaque assay sampling in the Western English Channel (WEC), where diatoms frequently bloom. Unexpectedly, peaks in detection did not occur during characteristic spring diatom blooms, but coincided with a winter bloom of Coscinodiscus, suggesting that these bacteria likely influence distinct diatom host populations. We isolated multiple bacterial antagonists, spanning 4 classes and 10 bacterial orders. Notably, a diatom attaching Roseobacter Ponticoccus alexandrii was isolated multiple times, indicative of a persistent environmental presence. Moreover, many isolates had no prior reports of antagonistic activity towards diatoms. We verified diatom growth inhibitory effects of eight isolates. In all cases tested, these effects were activated by pre-exposure to diatom organic matter. Discovery of widespread 'cryptic' antagonistic activity indicates that bacterial pathogenicity towards diatoms is more prevalent than previously recognised. Finally, examination of the global biogeography of WEC antagonists revealed co-occurrence patterns with diatom host populations in marine waters globally.
Assuntos
Diatomáceas , Microalgas , Ecossistema , Estações do Ano , BactériasRESUMO
Changing patterns in diversity are a feature of many habitats, with seasonality a major driver of ecosystem structure and function. In coastal marine plankton-based ecosystems, seasonality has been established through long-term time-series of bacterioplankton and protists. Alongside these groups, fungi also inhabit coastal marine ecosystems. If and how marine fungi show long-term intra- and inter-annual diversity patterns is unknown, preventing a comprehensive understanding of marine fungal ecology. Here, we use a 17-year environmental DNA time-series from the English Channel to determine long-term marine fungal diversity patterns. We show that fungal community structure progresses at seasonal and monthly scales and is only weakly related to environmental parameters. Communities restructured every 52-weeks suggesting long-term stability in diversity patterns. Some major marine fungal genera have clear inter-annual recurrence patterns, re-appearing in the annual cycle at the same period. Low relative abundance taxa that are likely non-marine show seasonal input to the coastal marine ecosystem suggesting land-sea exchange regularly takes place. Our results demonstrate long-term intra- and inter-annual marine fungal diversity patterns. We anticipate this study could form the basis for better understanding the ecology of marine fungi and how they fit in the structure and function of the wider coastal marine ecosystem.
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DNA Ambiental , DNA Fúngico , Ecossistema , Ecologia , Estações do Ano , Água do Mar/microbiologiaRESUMO
We present a genome assembly from a Metschnikowia zobellii culture (a marine yeast; Ascomycota; Saccharomycetes; Saccharomycetales; Metschnikowiaceae). The genome sequence is 13.6 megabases in span. Most of the assembly is scaffolded into 5 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 51.12 kilobases in length.
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Multiomics approaches need to be applied in the central Arctic Ocean to benchmark biodiversity change and to identify novel species and their genes. As part of MOSAiC, EcoOmics will therefore be essential for conservation and sustainable bioprospecting in one of the least explored ecosystems on Earth.
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Benchmarking , Ecossistema , Regiões Árticas , Biodiversidade , Oceanos e MaresRESUMO
The chytrids (phylum Chytridiomycota) are a major fungal lineage of ecological and evolutionary importance. Despite their importance, many fundamental aspects of chytrid developmental and cell biology remain poorly understood. To address these knowledge gaps, we combined quantitative volume electron microscopy and comparative transcriptome profiling to create an 'atlas' of the cellular and molecular basis of the chytrid life cycle, using the model chytrid Rhizoclosmatium globosum. From our developmental atlas, we describe the transition from the transcriptionally inactive free-swimming zoospore to the more biologically complex germling, and show that lipid processing is multifaceted and dynamic throughout the life cycle. We demonstrate that the chytrid apophysis is a compartmentalised site of high intracellular trafficking, linking the feeding/attaching rhizoids to the reproductive zoosporangium, and constituting division of labour in the chytrid cell plan. We provide evidence that during zoosporogenesis, zoospores display amoeboid morphologies and exhibit endocytotic cargo transport from the interstitial maternal cytoplasm. Taken together, our results reveal insights into chytrid developmental biology and provide a basis for future investigations into non-dikaryan fungal cell biology.
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Ascomicetos , Evolução Biológica , FilogeniaRESUMO
Fungal symbionts of terrestrial plants are among the most widespread and well-studied symbioses, relatively little is known about fungi that are associated with macroalgae. To fill the gap in marine fungal taxonomy, we combined simple culture methods with amplicon sequencing to characterize the fungal communities associated with three brown (Sargassum muticum, Pelvetia canaliculata, and Himanthalia elongata) and two red (Mastocarpus stellatus and Chondrus crispus) macroalgae from one intertidal zone. In addition to characterizing novel fungal diversity, we tested three hypotheses: fungal diversity and community composition vary (i) among species distributed at different tidal heights, (ii) among tissue types (apices, mid-thallus, and stipe), and (iii) among "isomorphic" C. crispus life cycle stages. Almost 70% of our reads were classified as Ascomycota, 29% as Basidiomycota, and 1% that could not be classified to a phylum. Thirty fungal isolates were obtained, 18 of which were also detected with amplicon sequencing. Fungal communities differed by host and tissue type. Interestingly, P. canaliculata, a fucoid at the extreme high intertidal, did not show differences in fungal diversity across the thallus. As found in filamentous algal endophytes, fungal diversity varied among the three life cycle stages in C. crispus. Female gametophytes were also compositionally more dispersed as compared to the fewer variable tetrasporophytes and male gametophytes. We demonstrate the utility of combining relatively simple cultivation and sequencing approaches to characterize and study macroalgal-fungal associations and highlight the need to understand the role of fungi in near-shore marine ecosystems.
Assuntos
Chondrus , Alga Marinha , Animais , Ecossistema , Endófitos , Estágios do Ciclo de VidaRESUMO
Marine fungi exist as three major cell types: unicellular yeasts, filamentous hyphae and zoosporic early-diverging forms, such as the Chytridiomycota (chytrids). To begin to understand the ecological and biogeochemical influence of these cell types within the wider context of other plankton groups, cell size and macromolecular composition must be assessed across all three cell types. Using a mass-balance approach to culture, we describe quantitative differences in substrate uptake and subsequent macromolecular distribution in three model marine fungi: the yeast Metschnikowia zobellii, the filamentous Epicoccum nigrum and chytrid Rhizophydium littoreum. We compared these model cell types with select oleaginous phytoplankton of specific biotechnological interest through metanalysis. We hypothesise that fungal cell types will maintain a significantly different macromolecular composition to one another and further represent an alternative grazing material to bacterioplankton and phytoplankton for higher trophic levels. Assessment of carbon substrate range and utilisation using phenotype arrays suggests that marine fungi have a wide substrate range. Fungi also process organic matter to an elevated-lipid macromolecular composition with reduced-protein content. Because of their size and increased lipid composition compared to other plankton groups, we propose that fungi represent a compositionally distinct, energy-rich grazing resource in marine ecosystems. We propose that marine fungi could act as vectors of organic matter transfer across trophic boundaries, and supplement our existing understanding of the microbial loop and carbon transfer in marine ecosystems.
RESUMO
The impact of selective predation of weaker individuals on the general health of prey populations is well-established in animal ecology. Analogous processes have not been considered at microbial scales despite the ubiquity of microbe-microbe interactions, such as parasitism. Here we present insights into the biotic interactions between a widespread marine thraustochytrid and a diatom from the ecologically important genus Chaetoceros. Physiological experiments show the thraustochytrid targets senescent diatom cells in a similar way to selective animal predation on weaker prey individuals. This physiology-selective targeting of 'unhealthy' cells appears to improve the overall health (i.e., increased photosynthetic quantum yield) of the diatom population without impacting density, providing support for 'healthy herd' dynamics in a protist-protist interaction, a phenomenon typically associated with animal predators and their prey. Thus, our study suggests caution against the assumption that protist-protist parasitism is always detrimental to the host population and highlights the complexity of microbial interactions.
Assuntos
Fitoplâncton , Comportamento Predatório , Animais , Ecologia , Eucariotos , Cadeia Alimentar , Humanos , Dinâmica Populacional , SimbioseRESUMO
The phylum Chytridiomycota (the "chytrids") is an early-diverging, mostly unicellular, lineage of fungi that consists of significant aquatic saprotrophs, parasites, and pathogens, and is of evolutionary interest because its members retain biological traits considered ancestral in the fungal kingdom. While the existence of aquatic chytrids has long been known, their fundamental biology has received relatively little attention. We are beginning to establish a detailed understanding of aquatic chytrid diversity and insights into their ecological functions and prominence. However, the underpinning biology governing their aquatic ecological activities and associated core processes remain largely understudied and therefore unresolved. Many biological questions are outstanding for aquatic chytrids. What are the mechanisms that control their development and life cycle? Which core processes underpin their aquatic influence? What can their biology tell us about the evolution of fungi and the wider eukaryotic tree of life? We propose that the field of aquatic chytrid ecology could be further advanced through the improved understanding of chytrid biology, including the development of model aquatic chytrids and targeted studies using culture-independent approaches.
RESUMO
Microbial colonization and degradation of particulate organic matter (POM) are important processes that influence the structure and function of aquatic ecosystems. Although POM is readily used by aquatic fungi and bacteria, there is a limited understanding of POM-associated interactions between these taxa, particularly for early-diverging fungal lineages. Using a model ecological system with the chitin-degrading freshwater chytrid fungus Rhizoclosmatium globosum and chitin microbeads, we assessed the impacts of chytrid fungi on POM-associated bacteria. We show that the presence of chytrids on POM alters concomitant bacterial community diversity and structure, including differing responses between chytrid life stages. We propose that chytrids can act as ecosystem facilitators through saprotrophic feeding by producing 'public goods' from POM degradation that modify bacterial POM communities. This study suggests that chytrid fungi have complex ecological roles in aquatic POM degradation not previously considered, including the regulation of bacterial colonization, community succession and subsequent biogeochemical potential.
Assuntos
Ecossistema , Material Particulado , Bactérias , Quitridiomicetos , FungosRESUMO
Key to the ecological prominence of fungi is their distinctive cell biology, our understanding of which has been principally based on dikaryan hyphal and yeast forms. The early-diverging Chytridiomycota (chytrids) are ecologically important and a significant component of fungal diversity, yet their cell biology remains poorly understood. Unlike dikaryan hyphae, chytrids typically attach to substrates and feed osmotrophically via anucleate rhizoids. The evolution of fungal hyphae appears to have occurred from rhizoid-bearing lineages and it has been hypothesized that a rhizoid-like structure was the precursor to multicellular hyphae. Here, we show in a unicellular chytrid, Rhizoclosmatium globosum, that rhizoid development exhibits striking similarities with dikaryan hyphae and is adaptive to resource availability. Rhizoid morphogenesis exhibits analogous patterns to hyphal growth and is controlled by ß-glucan-dependent cell wall synthesis and actin polymerization. Chytrid rhizoids growing from individual cells also demonstrate adaptive morphological plasticity in response to resource availability, developing a searching phenotype when carbon starved and spatial differentiation when interacting with particulate organic matter. We demonstrate that the adaptive cell biology and associated developmental plasticity considered characteristic of hyphal fungi are shared more widely across the Kingdom Fungi and therefore could be conserved from their most recent common ancestor.
Assuntos
Quitridiomicetos/fisiologia , Hifas/crescimento & desenvolvimento , Fungos , MorfogêneseRESUMO
Mycoplankton are widespread components of marine ecosystems, yet the full extent of their functional role remains poorly known. Marine mycoplankton are likely functionally analogous to their terrestrial counterparts, including performing saprotrophy and degrading high-molecular weight organic substrates using carbohydrate-active enzymes (CAZymes). We investigated the prevalence of transcribed oceanic fungal CAZyme genes using the Marine Atlas of Tara Ocean Unigenes database. We revealed an abundance of unique transcribed fungal glycoside hydrolases in the open ocean, including a particularly high number that act upon cellulose in surface waters and the deep chlorophyll maximum (DCM). A variety of other glycoside hydrolases acting on a range of biogeochemically important polysaccharides including ß-glucans and chitin were also found. This analysis demonstrates that mycoplankton are active saprotrophs in the open ocean and paves the way for future research into the depth-dependent roles of marine fungi in oceanic carbon cycling, including the biological carbon pump.
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Ecossistema , Glicosídeo Hidrolases , Eucariotos , Glicosídeo Hidrolases/genética , Glicosídeos , Oceanos e MaresRESUMO
Invertebrate activities in sediments, predominantly the redistribution of particles and porewater, are well-known to regulate the structure of associated microbial assemblages; however, relatively little attention has been given to the effects of sediment ingestion, gut passage and excretion by deposit-feeding invertebrates. Here, we use high-throughput sequencing and quantitative PCR to examine how passage through the gut of the marine polychaete Hediste diversicolor affects the structure of bacterial and archaeal assemblages and the abundance of nitrogen cycling taxa. We show that the digestive tract of H. diversicolor contains unique transitory microbial assemblages that, during gut passage, become more like the surrounding sediment assemblages. Enrichment of similar microbial taxa in both the hindgut and the burrow wall suggest that these transitory gut assemblages may influence the composition of the local sediment community. The hindgut of H. diversicolor also forms a reservoir for unique ammonia-oxidising archaeal taxa. Furthermore, distinct microbial assemblages on external polychaete surfaces suggest that deposit-feeding invertebrates act as vectors that transport microbes between sediment patches. Collectively, these findings suggest that the passage of sediment and associated microbial assemblages through the gut of deposit feeding invertebrates is likely to play a significant role in regulating sediment microbial assemblages and biogeochemical functioning.
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Archaea/isolamento & purificação , Bactérias/isolamento & purificação , Microbioma Gastrointestinal , Sedimentos Geológicos/microbiologia , Poliquetos/microbiologia , Amônia/metabolismo , Animais , Archaea/classificação , Archaea/genética , Archaea/metabolismo , Bactérias/classificação , Bactérias/genética , Bactérias/metabolismo , Ciclo do Nitrogênio , FilogeniaRESUMO
Fungi are phylogenetically and functionally diverse ubiquitous components of almost all ecosystems on Earth, including aquatic environments stretching from high montane lakes down to the deep ocean. Aquatic ecosystems, however, remain frequently overlooked as fungal habitats, although fungi potentially hold important roles for organic matter cycling and food web dynamics. Recent methodological improvements have facilitated a greater appreciation of the importance of fungi in many aquatic systems, yet a conceptual framework is still missing. In this Review, we conceptualize the spatiotemporal dimensions, diversity, functions and organismic interactions of fungi in structuring aquatic food webs. We focus on currently unexplored fungal diversity, highlighting poorly understood ecosystems, including emerging artificial aquatic habitats.
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Ecossistema , Fungos/isolamento & purificação , Microbiologia da Água , Antibiose , Biomassa , Cadeia Alimentar , Fungos/classificação , Fungos/genéticaRESUMO
Terrestrial fungi play critical roles in nutrient cycling and food webs and can shape macroorganism communities as parasites and mutualists. Although estimates for the number of fungal species on the planet range from 1.5 to over 5 million, likely fewer than 10% of fungi have been identified so far. To date, a relatively small percentage of described species are associated with marine environments, with â¼1,100 species retrieved exclusively from the marine environment. Nevertheless, fungi have been found in nearly every marine habitat explored, from the surface of the ocean to kilometers below ocean sediments. Fungi are hypothesized to contribute to phytoplankton population cycles and the biological carbon pump and are active in the chemistry of marine sediments. Many fungi have been identified as commensals or pathogens of marine animals (e.g., corals and sponges), plants, and algae. Despite their varied roles, remarkably little is known about the diversity of this major branch of eukaryotic life in marine ecosystems or their ecological functions. This perspective emerges from a Marine Fungi Workshop held in May 2018 at the Marine Biological Laboratory in Woods Hole, MA. We present the state of knowledge as well as the multitude of open questions regarding the diversity and function of fungi in the marine biosphere and geochemical cycles.
Assuntos
Organismos Aquáticos/classificação , Organismos Aquáticos/isolamento & purificação , Biodiversidade , Fungos/classificação , Fungos/isolamento & purificação , Sedimentos Geológicos/microbiologia , Água do Mar/microbiologiaRESUMO
Sediment nitrogen cycling is a network of microbially mediated biogeochemical processes that are vital in regulating ecosystem functioning. Mucopolysaccharides (mucus) are produced by many invertebrates and have the potential to be an important source of organic carbon and nitrogen to sediment microorganisms. At present, we have limited understanding of how mucopolysaccharide moderates total sediment microbial communities and specific microbial functional groups that drive nitrogen cycling processes. To start addressing this knowledge gap, sediment slurries were incubated with and without Hediste diversicolor mucus. Changes in dissolved inorganic nitrogen (ammonia, nitrite and nitrate) concentrations and bacterial and archaeal community diversity were assessed. Our results showed that mucopolysaccharide addition supported a more abundant and distinct microbial community. Moreover, mucus stimulated the growth of bacterial and archaeal ammonia oxidisers, with a concomitant increase in nitrite and nitrate. Hediste diversicolor mucopolysaccharide appears to enhance sediment nitrification rates by stimulating and fuelling nitrifying microbial groups. We propose that invertebrate mucopolysaccharide secretion should be considered as a distinct functional trait when assessing invertebrate contributions to sediment ecosystem function. By including this additional trait, we can improve our mechanistic understanding of invertebrate-microbe interactions in nitrogen transformation processes and provide opportunity to generate more accurate models of global nitrogen cycling.