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Mason, O. U.

Publications and source records attributed to Mason, O. U..

9 recordsLinked to original sources

Genomic and metatranscriptomic analyses reveal an active microbial hydrocarbon cycle in the photic zone

Natural hydrocarbon seeps and hydrocarbons resulting from human activities are the primary conduits by which oil enters the sea. Marine Cyanobacteria, among the most abundant photosynthetic organisms in the world, produce alkanes, an additional hydrocarbon source to the sea. Alkane production proceeds via metabolism of fatty acid intermediates with a fatty acyl-ACP reductase (FAAR) and an aldehyde-deformylating oxygenase (ADO). These alkanes can be consumed with alkane hydroxylases, including alkane 1-monooxygenase (alkB). The production and consumption of alkanes in the photic zone is termed the short-term hydrocarbon cycle (STHC). Yet, an active STHC has not been substantiated through gene expression analyses. To determine if the STHC is active in the marine photic zone we evaluated over 9000 genomes to which metatranscriptome reads from a site in the Gulf of Mexico were recruited. In these samples, FAAR and ADO expression was dominated by Prochlorococcus and to a lesser extent Synechococcus. Bacterial alkane consumption via alkB was dominated by Pseudomonadota, SAR324, and Bacteroidota alkB gene expression. Additionally, archaeal alkane consumption utilizing this same n-alkane degradation pathway was observed in the transcript data by Thermoplasmatota, classified as Marine Group II and III, the most abundant planktonic archaeal groups. Active production of alkanes in the photic zone would be an important component of marine hydrocarbon cycle and more broadly of carbon cycling. Further, consumption of hydrocarbons, regardless of source, is a fundamentally important ecosystem cleanup service provided by microbes in the ocean. ImportanceHydrocarbons in the long-term hydrocarbon cycle (LTHC) are produced over long-time scales. In comparison, hydrocarbons, specifically n-alkanes, are produced on short time scales by Cyanobacteria as part of basic cellular processes in the short-term hydrocarbon cycle (STHC). Cyanobacterial production of n-alkanes leads to an additional annual input of more than 100 million tons of hydrocarbons to the ocean. Despite the difference in time scale and source, these hydrocarbon cycles are intrinsically linked by microbes that consume n-alkanes using the same pathways for degradation. Here we show that the production and consumption in the STHC is an active cycle in the sunlit ocean, as determined by analysis of genomes and metatranscriptomes. Importantly an active STHC could support a population of alkane degrading bacteria, enabling a rapid response to oil input from a geological reservoir as part of the LTHC, through natural or anthropogenic activities, with implications for bioremediation and ultimately for marine ecosystem health.

microbiology↗

Dissolved oxygen concentrations influence microbial diversity, abundance and dominant players in an oxygen minimum zone

Expansion of marine global oxygen minimum zones (OMZs) can have profound impacts on resident macrofauna. Less obvious is the influence OMZs will have on the diversity and abundance of planktonic microbes. This is particularly true in understudied OMZs such as the northern Benguela Upwelling System (nBUS). Here, we analyzed the influence of oxygen concentrations on the microbial community in the nBUS OMZ using 16S rRNA gene (iTag) sequence data. In the nBUS oxygen was a primary driver influencing microbial community structure and diversity. Diversity was highest in dysoxic samples and lowest in suboxic samples, which was primarily due to changes in community evenness in relationship to oxygen concentrations. For example, evenness decreased in suboxic samples due to oscillations in the abundance of microbial groups such as Thioglobaceae (SUP05), which was found to be the most abundant microbe in the nBUS OMZ and significantly increased in abundance as oxygen decreased. This finding prompted an analysis of 217 publicly available medium to high quality Thioglobaceae genomes, including cultured representatives, from the nBUS and other OMZs. Genome annotation of these Thioglobaceae indicated important roles in carbon cycling, sulfur oxidation and denitrification. Importantly, few Thioglobaceae possess the genetic potential to carry out complete denitrification, as most lack the gene that codes for nitrous oxide reductase (NosZ), which converts nitrous oxide (N2O), a potent greenhouse gas, to nitrogen gas. As OMZs expand in size and severity, decreasing microbial diversity and a concomitant increase in Thioglobaceae abundances, could lead to enhanced N2O production through incomplete denitrification. ImportanceHere, we found that microbial diversity decreased significantly with declining oxygen concentrations in the nBUS OMZ. However, one microbial group, the Thioglobaceae, was most abundant when oxygen was lowest. This group is able to support its growth through sulfur oxidation using either oxygen or nitrate (denitrification). A comprehensive genomic analysis of Thioglobaceae in the nBUS and in the global ocean revealed that few have the capacity to carry out complete denitrification, with the final step in this process often missing in these genomes. This incomplete pathway is consequential, as it can be an important source of nitrous oxide, particularly in marine OMZs such as the understudied nBUS. Collectively, this study provides new information on an OMZ, and definitively links an important microbial pathway, incomplete denitrification, to a particular and highly abundant group of microbes that appear to have a strong response to declining oxygen concentrations in the marine environment.

microbiology↗

Denitrification genes in SAR11 and other ubiquitous lineages of marine bacteria isolated from the northern Benguela Upwelling System

Denitrification is a microbial process that leads to nitrogen loss from marine oxygen minimum zones (OMZs). The complete metabolic pathway for denitrification reduces nitrate to dinitrogen gas in four sequential steps. Many anaerobic and facultatively anaerobic bacteria are capable of the initial step of nitrate reduction to nitrite. Far fewer reduce nitrite to nitric oxide, nitrous oxide, or dinitrogen gas. In this study, we cultured and sequenced the complete genomes of 24 bacteria isolated from low dissolved oxygen waters (DO = 24 {micro}M) in the northern Benguela Upwelling System (nBUS) OMZ to identify facultatively anaerobic bacteria with the genetic potential to contribute to denitrification. Most of the isolates obtained from the nBUS have denitrification genes (79%). They include several new species in the order Pelagibacterales (SAR11), as well as representatives from a previously uncultured family of Arenicellales (UBA868), a previously uncultured genus of Paracoccaceae, and a previously undescribed genus of Porticoccaceae. All ten nBUS SAR11 have a previously unidentified genomic region that codes for a copper-containing nitrite reductase (nirK), suggesting that they have the potential to contribute to nitrogen loss by respiring nitrite to nitric oxide. Significance StatementVast genomic diversity has confounded sequencing efforts to identity the potential for marine bacteria to contribute to denitrification in marine oxygen minimum zones (OMZs). To identify facultatively anaerobic microbes with the genetic potential to contribute to marine nitrogen loss, we cultured and sequenced the complete genomes of bacteria from low-oxygen waters of the northern Benguela Upwelling System. Complete genomes allowed for a comprehensive analysis of denitrification. Most bacterial isolates, including all ten SAR11, have the genetic potential to contribute to denitrification. This suggests that some of the most abundant lineages of marine bacteria in the oceans are adapted to anoxic conditions in OMZs and may have a more direct role in marine nitrogen loss than previously suspected.

microbiology↗

Uncovering novel functions of the enigmatic, abundant and active Anaerolineae in a salt marsh ecosystem

Anaerolineae, particularly uncultured representatives, are one of the most abundant microbial groups in coastal salt marshes, dominating the belowground rhizosphere, where over half of plant biomass production occurs. However, this class generally remains poorly understood, particularly in a salt marsh context. Here, novel Anaerolineae metagenome assembled genomes (MAGs) were generated from the salt marsh rhizosphere representing Anaerolineales, Promineifilales, JAAYZQ01, B4-G1, JAFGEY01, UCB3, and Caldilineales orders. Metagenome and metatranscriptome reads were mapped to annotated MAGs, revealing nearly all Anaerolineae encoded and transcribed genes required for oxidation of simple sugars to complex carbon compounds, fermentation, and carbon fixation. Further, the majority of Anaerolineae expressed genes involved in anaerobic and aerobic respiration and secondary metabolite production. The data revealed that the belowground salt marsh Anaerolineae in the rhizosphere are important players in carbon cycling, including degradation of simple carbon compounds to more recalcitrant plant material, such as cellulose, using a diversity of electron acceptors and represent an unexplored reservoir of novel secondary metabolites. ImportanceGiven that coastal salt marshes are recognized as biogeochemical hotspots, it is fundamentally important to understand the functional role of the microbiome in this ecosystem. In particular, Anaerolineae are abundant members of the salt marsh rhizosphere and have been identified as core microbes, suggesting they play a particularly important functional role. Yet, little is known about the metabolic pathways encoded and expressed in this abundant salt marsh clade. Using an omics based approach we determined that Anaerolineae are capable of oxidizing a range of carbon compounds, including simple sugars to complex carbon compounds, while also encoding fermentation and carbon fixation. Surprisingly, Anaerolineae encoded and transcribed genes involved in aerobic respiration, which was unexpected given the reduced nature of the salt marsh rhizosphere. Finally, the majority of Anaerolineae appear to be involved in secondary metabolite production, suggesting that this group represents an unexplored reservoir of novel and important secondary metabolites.

microbiology↗

Novel, active, and uncultured hydrocarbon degrading microbes in the ocean

Given the vast quantity of oil and gas input to the marine environment annually, hydrocarbon degradation by marine microorganisms is an essential ecosystem service. Linkages between taxonomy and hydrocarbon degradation capabilities are largely based on cultivation studies, leaving a knowledge gap regarding the intrinsic ability of uncultured marine microbes to degrade hydrocarbons. To address this knowledge gap, metagenomic sequence data from the Deepwater Horizon (DWH) oil spill deep-sea plume was assembled to which metagenomic and metatranscriptomic reads were mapped. Assembly and binning produced new DWH metagenome assembled genomes that were evaluated along with their close relatives, all of which are from the marine environment (38 total). These analyses revealed globally distributed hydrocarbon degrading microbes with clade specific substrate degradation potentials that have not been reported previously. For example, methane oxidation capabilities were identified in all Cycloclasticus. Further, all Bermanella encoded and expressed genes for non-gaseous n-alkane degradation; however, DWH Bermanella encoded alkane hydroxylase, not alkane 1-monooxygenase. All but one previously unrecognized DWH plume members in the SAR324 and UBA11654 coded for aromatic hydrocarbon degradation. In contrast, Colwellia were diverse in the hydrocarbon substrates they could degrade. All clades encoded nutrient acquisition strategies and response to cold temperatures, while sensory and acquisition capabilities were clade specific. These novel insights regarding hydrocarbon degradation by uncultured planktonic microbes provided missing data, allowing for better prediction of the fate of oil and gas when hydrocarbons are input to the ocean, leading to a greater understanding of the ecological consequences to the marine environment. ImportanceMicrobial degradation of hydrocarbons is a critically important process promoting ecosystem health, yet much of what is known about this process is based on physiological experiments with a few hydrocarbon substrates and cultured microbes. Thus, the ability to degrade the diversity of hydrocarbons that comprise oil and gas by microbes in the environment, particularly in the ocean, is not well characterized. Therefore, this study aimed to utilize non-cultivation based omics data to explore novel genomes of uncultured marine microbes involved in degradation of oil and gas. Analyses of newly assembled metagenomic data and metagenomic and metatranscriptomic read recruitment revealed globally distributed hydrocarbon degrading marine microbes with clade specific substrate degradation potentials that have not been previously reported. This new understanding of oil and gas degradation by uncultured marine microbes suggested that the global ocean harbors a diversity of hydrocarbon degrading Bacteria, that can act as primary agents regulating ecosystem health.

microbiology↗

New insights into the influence of plant and microbial diversity on denitrification rates in a salt marsh

Coastal salt marshes are some of the most productive ecosystems on Earth, providing numerous services such as soil carbon storage, flood protection and nutrient filtering, several of which are mediated by the sediment microbiome associated with marsh vegetation. Here, nutrient filtering (nitrate removal through denitrification) was examined by determining microbial community structure (16S rRNA gene iTag sequencing), diversity, denitrification rates and metabolic potential (assembled metagenomic sequences) in collocated patches of Spartina alterniflora (Spartina) and Juncus roemerianus (Juncus) sediments. The iTag data showed that diversity and richness in Spartina and Juncus sediment microbial communities were highly similar. However, microbial community evenness differed significantly, with the most even communities observed in Juncus sediments. Further, denitrification rates were significantly higher in Juncus compared to Spartina, suggesting oscillations in microbial abundances and in particular the core microbiome identified herein, along with plant diversity influence marsh nitrogen (N) removal. Amplicon and assembled metagenome sequences pointed to a potentially important, yet unappreciated Planctomycetes role in N removal in the salt marsh. Thus, perturbations, such as sea-level rise, that can alter marsh vegetation distribution could impact microbial diversity and may ultimately influence the ecologically important ecosystem functions the marsh sediment microbiome provides.

microbiology↗

Host and environmental determinants of microbial community structure in the marine phyllosphere

Although seagrasses are economically and ecologically critical species, little is known about their blade surface microbial communities and how these communities relate to the plant host. To determine microbial community composition and diversity on seagrass blade surfaces and in the surrounding seawater,16S rRNA gene sequencing (iTag) was used for samples collected at five sites along a gradient of freshwater input in the northern Gulf of Mexico on three separate sampling dates. Additionally, seagrass surveys were performed and environmental parameters were measured to characterize host characteristics and the abiotic conditions at each site. Results showed that Thalassia testudinum (turtle grass) blades hosted unique microbial communities that were distinct in composition and diversity from the water column. Additionally, results suggested that environmental conditions, including water depth, salinity, and temperature, were the major driver of community structure as blade surface microbial communities varied among sites and over sampling dates. Host condition may be a secondary driver of community structure as compositional changes were also correlated with host characteristics, including leaf growth rates and blade nutrient composition, Additionally, 21 microorganisms from five phyla (Cyanobacteria, Proteobacteria, Planctomycetes, Chloroflexi, and Bacteroidetes) were present in all blade surface samples and may represent a core community for T. testudinum. Members of this core community may have ecological importance for determining community structure or in performing key community functions. This study provides new insights and understanding of the processes that influence the structure of marine phyllosphere communities, how these microbial communities relate to their host, and their role as a part of the seagrass holobiont, which is an important contribution given the current decline of seagrass coverage worldwide.

microbiology↗

Decoding bacterioplankton metabolism in the northern Gulf of Mexico Dead Zone

Marine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called dead zones, are increasing in number and severity around the globe with deleterious effects on ecology and economics. One of the largest of these coastal dead zones occurs on the continental shelf of the northern Gulf of Mexico (nGOM), which results from eutrophication-enhanced bacterioplankton respiration and strong seasonal stratification. Previous research in this dead zone revealed the presence of multiple cosmopolitan bacterioplankton lineages that have eluded cultivation, and thus their metabolic roles in this ecosystem remain unknown. We used a coupled shotgun metagenomic and metatranscriptomic approach to determine the metabolic potential of Marine Group II Euryarchaeota, SAR406, and SAR202. We recovered multiple high-quality, nearly complete genomes from all three groups as well as those belonging to Candidate Phyla usually associated with anoxic environments-Parcubacteria (OD1) and Peregrinibacteria. Two additional groups with putative assignments to ACD39 and PAUC34f supplement the metabolic contributions by uncultivated taxa. Our results indicate active metabolism in all groups, including prevalent aerobic respiration, with concurrent expression of genes for nitrate reduction in SAR406 and SAR202, and dissimilatory nitrite reduction to ammonia and sulfur reduction by SAR406. We also report a variety of active heterotrophic carbon processing mechanisms, including degradation of complex carbohydrate compounds by SAR406, SAR202, ACD39, and PAUC34f. Together, these data help constrain the metabolic contributions from uncultivated groups in the nGOM during periods of low DO and suggest roles for these organisms in the breakdown of complex organic matter.\n\nImportanceDead zones receive their name primarily from the reduction of eukaryotic macrobiota (demersal fish, shrimp, etc.) that are also key coastal fisheries. Excess nutrients contributed from anthropogenic activity such as fertilizer runoff result in algal blooms and therefore ample new carbon for aerobic microbial metabolism. Combined with strong stratification, microbial respiration reduces oxygen in shelf bottom waters to levels unfit for many animals (termed hypoxia). The nGOM shelf remains one of the largest eutrophication-driven hypoxic zones in the world, yet despite its potential as a model study system, the microbial metabolisms underlying and resulting from this phenomenon--many of which occur in bacterioplankton from poorly understood lineages--have received only preliminary study. Our work details the metabolic potential and gene expression activity for uncultivated lineages across several low DO sites in the nGOM, improving our understanding of the active biogeochemical cycling mediated by these \"microbial dark matter\" taxa during hypoxia.

microbiology↗

Metabolic and spatio-taxonomic response of uncultivated seafloor bacteria following the Deepwater Horizon oil spill

The release of 700 million liters of oil into the Gulf of Mexico over a few months in 2010 produced dramatic changes in the microbial ecology of the water and sediment. Previous 4 studies have examined the phylogeny and function of these changes, but until now a 5 fundamental examination of the extant hydrocarbon metabolisms that supported these 6 changes had not been performed. Here, we reconstructed the genomes of 57 widespread 7 uncultivated bacteria from post spill sediments, and recovered their gene expression 8 pattern across the seafloor. These genomes comprised a common collection of bacteria 9 that were highly enriched in heavily affected sediments around the wellhead. While rare in distal sediments, some members were still detectable at sites up to 60 km away. Many of these genomes exhibited phylogenetic clustering indicative of common trait selection by the environment, and within half we identified 264 genes associated with hydrocarbon degradation. Observed alkane degradation ability was near ubiquitous among candidate hydrocarbon degraders, while just 3 harbored elaborate gene inventories for the degradation of alkanes and (poly)aromatic hydrocarbons. Differential gene expression profiles revealed a spill-promoted microbial sulfur cycle alongside gene up-regulation associated with polyaromatic hydrocarbon degradation. Gene expression associated with alkane degradation was widespread, although active alkane degrader identities changed along the pollution gradient. The resulting analysis suggests a broad metabolic capacity to respond to oil exists across a large array of usually rare bacteria.

microbiology↗