Marine Group II (MGII) archaea represent the most abundant planktonic archaeal group in ocean surface waters, but our understanding of the group has been limited by a lack of cultured representatives ...and few sequenced genomes. Here, we conducted a comparative phylogenomic analysis of 270 recently available MGII metagenome-assembled genomes (MAGs) to investigate their evolution and ecology. Based on a rank-normalised genome phylogeny, we propose that MGII is an order-level lineage for which we propose the name Candidatus Poseidoniales (after Gr. n. Poseidon, God of the sea), comprising the families Candidatus Poseidonaceae fam. nov. (formerly subgroup MGIIa) and Candidatus Thalassarchaeaceae fam. nov. (formerly subgroup MGIIb). Within these families, 21 genera could be resolved, many of which had distinct biogeographic ranges and inferred nutrient preferences. Phylogenetic analyses of key metabolic functions suggest that the ancestor of Ca. Poseidoniales was a surface water-dwelling photoheterotroph that evolved to occupy multiple related ecological niches based primarily on spectral tuning of proteorhodopsin genes. Interestingly, this adaptation appears to involve an overwrite mechanism whereby an existing single copy of the proteorhodopsin gene is replaced by a horizontally transferred copy, which in many instances should allow an abrupt change in light absorption capacity. Phototrophy was lost entirely from five Ca. Poseidoniales genera coinciding with their adaptation to deeper aphotic waters. We also report the first instances of nitrate reductase in two genera acquired via horizontal gene transfer (HGT), which was a potential adaptation to oxygen limitation. Additional metabolic traits differentiating families and genera include flagellar-based adhesion, transporters, and sugar, amino acid, and peptide degradation. Our results suggest that HGT has shaped the evolution of Ca. Poseidoniales to occupy a variety of ecological niches and to become the most successful archaeal lineage in ocean surface waters.
Microbial diversity has been extensively explored in reef-building corals. However, the functional roles of coral-associated microorganisms remain poorly elucidated. Here, we recover 191 bacterial ...and 10 archaeal metagenome-assembled genomes (MAGs) from the coral Acropora kenti (formerly A. tenuis) and adjacent seawater, to identify microbial functions and metabolic interactions within the holobiont. We show that 82 MAGs were specific to the A. kenti holobiont, including members of the Pseudomonadota, Bacteroidota, and Desulfobacterota. A. kenti-specific MAGs displayed significant differences in their genomic features and functional potential relative to seawater-specific MAGs, with a higher prevalence of genes involved in host immune system evasion, nitrogen and carbon fixation, and synthesis of five essential B-vitamins. We find a diversity of A. kenti-specific MAGs encode the biosynthesis of essential amino acids, such as tryptophan, histidine, and lysine, which cannot be de novo synthesised by the host or Symbiodiniaceae. Across a water quality gradient spanning 2° of latitude, A. kenti microbial community composition is correlated to increased temperature and dissolved inorganic nitrogen, with corresponding enrichment in molecular chaperones, nitrate reductases, and a heat-shock protein. We reveal mechanisms of A. kenti-microbiome-symbiosis on the Great Barrier Reef, highlighting the interactions underpinning the health of this keystone holobiont.
Microbial functioning on marine plastic surfaces has been poorly documented, especially within cold climates where temperature likely impacts microbial activity and the presence of ...hydrocarbonoclastic microorganisms. To date, only two studies have used metaproteomics to unravel microbial genotype-phenotype linkages in the marine 'plastisphere', and these have revealed the dominance of photosynthetic microorganisms within warm climates. Advancing the functional representation of the marine plastisphere is vital for the development of specific databases cataloging the functional diversity of the associated microorganisms and their peptide and protein sequences, to fuel biotechnological discoveries. Here, we provide a comprehensive assessment for plastisphere metaproteomics, using multi-omics and data mining on thin plastic biofilms to provide unique insights into plastisphere metabolism. Our robust experimental design assessed DNA/protein co-extraction and cell lysis strategies, proteomics workflows, and diverse protein search databases, to resolve the active plastisphere taxa and their expressed functions from an understudied cold environment.
For the first time, we demonstrate the predominance and activity of hydrocarbonoclastic genera (Psychrobacter, Flavobacterium, Pseudomonas) within a primarily heterotrophic plastisphere. Correspondingly, oxidative phosphorylation, the citrate cycle, and carbohydrate metabolism were the dominant pathways expressed. Quorum sensing and toxin-associated proteins of Streptomyces were indicative of inter-community interactions. Stress response proteins expressed by Psychrobacter, Planococcus, and Pseudoalteromonas and proteins mediating xenobiotics degradation in Psychrobacter and Pseudoalteromonas suggested phenotypic adaptations to the toxic chemical microenvironment of the plastisphere. Interestingly, a targeted search strategy identified plastic biodegradation enzymes, including polyamidase, hydrolase, and depolymerase, expressed by rare taxa. The expression of virulence factors and mechanisms of antimicrobial resistance suggested pathogenic genera were active, despite representing a minor component of the plastisphere community.
Our study addresses a critical gap in understanding the functioning of the marine plastisphere, contributing new insights into the function and ecology of an emerging and important microbial niche. Our comprehensive multi-omics and comparative metaproteomics experimental design enhances biological interpretations to provide new perspectives on microorganisms of potential biotechnological significance beyond biodegradation and to improve the assessment of the risks associated with microorganisms colonizing marine plastic pollution. Video Abstract.
Corals and the reef ecosystems that they support are in global decline due to increasing anthropogenic pressures such as climate change
. However, effective reef conservation strategies are hampered ...by a limited mechanistic understanding of coral biology and the functional roles of the diverse microbial communities that underpin coral health
. Here, we present an integrated genomic characterization of the coral species Porites lutea and its microbial partners. High-quality genomes were recovered from P. lutea, as well as a metagenome-assembled Cladocopium C15 (the dinoflagellate symbiont) and 52 bacterial and archaeal populations. Comparative genomic analysis revealed that many of the bacterial and archaeal genomes encode motifs that may be involved in maintaining association with the coral host and in supplying fixed carbon, B-vitamins and amino acids to their eukaryotic partners. Furthermore, mechanisms for ammonia, urea, nitrate, dimethylsulfoniopropionate and taurine transformation were identified that interlink members of the holobiont and may be important for nutrient acquisition and retention in oligotrophic waters. Our findings demonstrate the critical and diverse roles that microorganisms play within the coral holobiont and underscore the need to consider all of the components of the holobiont if we are to effectively inform reef conservation strategies.
Australia's tropical waters represent predicted 'hotspots' for nitrogen (N2) fixation based on empirical and modelled data. However, the identity, activity and ecology of diazotrophs within this ...region are virtually unknown. By coupling DNA and cDNA sequencing of nitrogenase genes (nifH) with size-fractionated N2 fixation rate measurements, we elucidated diazotroph dynamics across the shelf region of the Arafura and Timor Seas (ATS) and oceanic Coral Sea during Austral spring and winter. During spring, Trichodesmium dominated ATS assemblages, comprising 60% of nifH DNA sequences, while Candidatus Atelocyanobacterium thalassa (UCYN-A) comprised 42% in the Coral Sea. In contrast, during winter the relative abundance of heterotrophic unicellular diazotrophs (δ-proteobacteria and γ-24774A11) increased in both regions, concomitant with a marked decline in UCYN-A sequences, whereby this clade effectively disappeared in the Coral Sea. Conservative estimates of N2 fixation rates ranged from <1 to 91 nmol l(-1) day(-1), and size fractionation indicated that unicellular organisms dominated N2 fixation during both spring and winter, but average unicellular rates were up to 10-fold higher in winter than in spring. Relative abundances of UCYN-A1 and γ-24774A11 nifH transcripts negatively correlated to silicate and phosphate, suggesting an affinity for oligotrophy. Our results indicate that Australia's tropical waters are indeed hotspots for N2 fixation and that regional physicochemical characteristics drive differential contributions of cyanobacterial and heterotrophic phylotypes to N2 fixation.
Research into the microbiomes of natural environments is changing the way ecologists and evolutionary biologists view the importance of microorganisms in ecosystem function. This is particularly ...relevant in ocean environments, where microorganisms constitute the majority of biomass and control most of the major biogeochemical cycles, including those that regulate Earth's climate. Coastal marine environments provide goods and services that are imperative to human survival and well-being (for example, fisheries and water purification), and emerging evidence indicates that these ecosystem services often depend on complex relationships between communities of microorganisms (the 'microbiome') and the environment or their hosts - termed the 'holobiont'. Understanding of coastal ecosystem function must therefore be framed under the holobiont concept, whereby macroorganisms and their associated microbiomes are considered as a synergistic ecological unit. Here, we evaluate the current state of knowledge on coastal marine microbiome research and identify key questions within this growing research area. Although the list of questions is broad and ambitious, progress in the field is increasing exponentially, and the emergence of large, international collaborative networks and well-executed manipulative experiments are rapidly advancing the field of coastal marine microbiome research.
Biological dinitrogen (N
) fixation is one mechanism by which specific microorganisms (diazotrophs) can ameliorate nitrogen (N) limitation. Historically, rates of N
fixation were believed to be ...limited outside of the low nutrient tropical and subtropical open ocean; however, emerging evidence suggests that N
fixation is also a significant process within temperate coastal waters. Using a combination of amplicon sequencing, targeting the nitrogenase reductase gene (
), quantitative
PCR, and
N
stable isotope tracer experiments, we investigated spatial patterns of diazotroph assemblage structure and N
fixation rates within the temperate coastal waters of southern Australia during Austral autumn and summer. Relative to previous studies in open ocean environments, including tropical northern Australia, and tropical and temperate estuaries, our results indicate that high rates of N
fixation (10-64 nmol L
d
) can occur within the large inverse estuary Spencer Gulf, while comparatively low rates of N
fixation (2 nmol L
d
) were observed in the adjacent continental shelf waters. Across the dataset, low concentrations of NO
/NO
were significantly correlated with the highest N
fixation rates, suggesting that N
fixation could be an important source of new N in the region as dissolved inorganic N concentrations are typically limiting. Overall, the underlying diazotrophic community was dominated by
sequences from Cluster 1 unicellular cyanobacteria of the UCYN-A clade, as well as non-cyanobacterial diazotrophs related to
, and Cluster 3 sulfate-reducing deltaproteobacteria. Diazotroph community composition was significantly influenced by salinity and SiO
concentrations, reflecting the transition from UCYN-A-dominated assemblages in the continental shelf waters, to Cluster 3-dominated assemblages in the hypersaline waters of the inverse estuary. Diverse, transitional diazotrophic communities, comprised of a mixture of UCYN-A and putative heterotrophic bacteria, were observed at the mouth and southern edge of Spencer Gulf, where the highest N
fixation rates were observed. In contrast to observations in other environments, no seasonal patterns in N
fixation rates and diazotroph community structure were apparent. Collectively, our findings are consistent with the emerging view that N
fixation within temperate coastal waters is a previously overlooked dynamic and potentially important component of the marine N cycle.
Discrepancies between bioavailable nitrogen (N) concentrations and phytoplankton growth rates in the oligotrophic waters of the Great Barrier Reef (GBR) suggest that undetermined N sources must play ...a significant role in supporting primary productivity. One such source could be biological dinitrogen (N
) fixation through the activity of "diazotrophic" bacterioplankton. Here, we investigated N
fixation and diazotroph community composition over 10° S of latitude within GBR surface waters. Qualitative N
fixation rates were found to be variable across the GBR but were relatively high in coastal, inner and outer GBR waters, reaching 68 nmol L
d
. Diazotroph assemblages, identified by amplicon sequencing of the
gene, were dominated by the cyanobacterium
, γ-proteobacteria from the Gamma A clade, and δ-proteobacterial phylotypes related to sulfate-reducing genera. However, diazotroph communities exhibited significant spatial heterogeneity, correlated with shifts in dissolved inorganic nutrient concentrations. Specifically, heterotrophic diazotrophs generally increased in relative abundance with increasing concentrations of phosphate and N, while
was proportionally more abundant when concentrations of these nutrients were low. This study provides the first in-depth characterization of diazotroph community composition and N
fixation dynamics within the oligotrophic, N-limited surface waters of the GBR. Our observations highlight the need to re-evaluate N cycling dynamics within oligotrophic coral reef systems, to include diverse N
fixing assemblages as a potentially significant source of dissolved N within the water column.
The taxonomy of marine plastisphere communities has been extensively studied, demonstrating the ubiquity of hydrocarbonoclastic bacteria of potential biotechnological significance. However, ...prokaryotic functioning on plastic surfaces has received limited attention, and the question of whether these microorganisms are active and expressing specific molecular mechanisms underpinning plastisphere colonisation remains to be addressed. The aim of this study was to investigate the plastic colonisation process, to identify the active taxa involved in biofilm formation and the mechanisms used to initiate colonisation. To achieve this, a marine plastisphere characterised by active hydrocarbonoclastic genera was used as the inoculum for a short-term microcosm experiment using virgin low-density polyethylene as the sole carbon source. Following incubation for 1 and 2 weeks (representing early and late colonisation, respectively), a taxonomic and comparative metaproteomic approach revealed a significant shift in plastisphere diversity and composition, yet highlighted stability in the predominance of active Proteobacteria spanning 16 genera, including Marinomonas, Pseudomonas, and Pseudoalteromonas. Relative quantification of 1762 proteins shared between the initial plastisphere inoculum, the microcosm plastisphere and the planktonic cells in the surrounding artificial seawater, provided insights into the differential regulation of proteins associated with plastisphere formation. This included the upregulation of proteins mediating cellular attachment in the plastisphere, for example flagellin expressed by Marinomonas, Cobetia, Pseudoalteromonas, and Pseudomonas, and curli expressed by Cobetia. In addition to the differential regulation of energy metabolism in Marinomonas, Psychrobacter, Pseudomonas and Cobetia within the plastisphere relative to the surrounding seawater. Further, we identified the upregulation of amino acid metabolism and transport, including glutamine hydrolysis to glutamate in Marinomonas and unclassified Halomonadaceae, potentially coupled to ammonia availability and oxidative stress experienced within the plastisphere. Our study provides novel insights into the dynamics of plastisphere formation and function, highlighting potential targets for regulating plastisphere growth to enhance plastic bioremediation processes.
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•Proteobacteria from 16 genera dominated the active plastisphere taxa.•Physiological, morphological, and metabolic pathways established plastic colonisation.•Energy and glutamine metabolism underpinned plastisphere and planktonic states.•Molecular mechanisms to enhance plastics bio-recycling were identified.
Abstract Postmortem studies have documented abnormalities in the dorsolateral prefrontal cortex (dlPFC) in depressed subjects. In this study we used magnetic resonance imaging to test for dlPFC ...volume differences between older depressed and non-depressed individuals. Eighty-eight subjects meeting DSM IV criteria for major depressive disorder and thirty-five control subjects completed clinical evaluations and cranial 3T magnetic resonance imaging. After tissue types were identified using an automated segmentation process, the dlPFC was measured in both hemispheres using manual delineation based on anatomical landmarks. Depressed subjects had significantly lower gray matter in the left and right dorsolateral prefrontal cortex (standardized to cerebral parenchyma) after controlling for age and sex. Our study confirmed the reduction of dorsolateral prefrontal cortex in elderly depressed subjects, especially in the gray matter. These regional abnormalities may be associated with psychopathological changes in late-life depression.
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