ABSTRACT
Dissolved organic phosphorus (DOP) contains compounds with phosphoester, phosphoanhydride, and phosphorus-carbon bonds. While DOP holds significant nutritional value for marine microorganisms, the bioavailability of each bond-class to the widespread cyanobacterium Synechococcus remains largely unknown. This study evaluates bond-class specific DOP utilization by Synechococcus strains from open and coastal oceans. Both strains exhibited comparable growth rates when provided phosphate, a phosphoanhydride [3-polyphosphate and 45-polyphosphate], or a DOP compound with both phosphoanhydride and phosphoester bonds (adenosine 5'-triphosphate). Growth rates on phosphoesters [glucose-6-phosphate, adenosine 5'-monophosphate, bis(4-methylumbelliferyl) phosphate] were variable, and neither strain grew on selected phosphorus-carbon compounds. Both strains hydrolyzed 3-polyphosphate, then adenosine 5'-triphosphate, and lastly adenosine 5'-monophosphate, exhibiting preferential enzymatic hydrolysis of phosphoanhydride bonds. The strains' exoproteomes contained phosphorus hydrolases, which combined with enhanced cell-free hydrolysis of 3-polyphosphate and adenosine 5'-triphosphate under phosphate deficiency, suggests active mineralization of phosphoanhydride bonds by these exoproteins. Synechococcus alkaline phosphatases presented broad substrate specificities, including activity toward the phosphoanhydride 3-polyphosphate, with varying affinities between strains. Collectively, these findings underscore the potentially significant role of compounds with phosphoanhydride bonds in Synechococcus phosphorus nutrition and highlight varied growth and enzymatic responses to molecular diversity within DOP bond-classes, thereby expanding our understanding of microbially mediated DOP cycling in marine ecosystems.
Subject(s)
Phosphorus , Synechococcus , Synechococcus/metabolism , Synechococcus/growth & development , Phosphorus/metabolism , Seawater/microbiology , Hydrolysis , Adenosine Triphosphate/metabolism , Polyphosphates/metabolismABSTRACT
Constitutive mixoplankton-plastid-bearing microbial eukaryotes capable of both phototrophy and phagotrophy-are ubiquitous in marine ecosystems and facilitate carbon transfer to higher trophic levels within aquatic food webs, which supports enhanced sinking carbon flux. However, the regulation of the relative contribution of photosynthesis and prey consumption remains poorly characterized. We investigated the transcriptional dynamics behind this phenotypic plasticity in the prasinophyte green alga Pterosperma cristatum. Based on what is known of other mixoplankton species that cannot grow without photosynthesis (obligate phototrophs), we hypothesized that P. cristatum uses phagotrophy to circumvent the restrictions imposed on photosynthesis by nutrient depletion, to obtain nutrients from ingested prey, and to maintain photosynthetic carbon fixation. We observed an increase in feeding as a response to nutrient depletion, coinciding with an upregulation of expression for genes involved in essential steps of phagocytosis including prey recognition, adhesion and engulfment, transport and maturation of food vacuoles, and digestion. Unexpectedly, genes involved in the photosynthetic electron transfer chain, pigment biosynthesis, and carbon fixation were downregulated as feeding increased, implying an abatement of photosynthesis. Contrary to our original hypothesis, our results therefore suggest that depletion of inorganic nutrients triggered an alteration of trophic behavior from photosynthesis to phagotrophy in P. cristatum. While this behavior distinguishes P. cristatum from other groups of constitutive mixoplankton, its physiological response aligns with recent discoveries from natural microbial communities. These findings indicate that mixoplankton communities in nutrient-limited oceans can regulate photosynthesis against bacterivory based on nutrient availability.
ABSTRACT
Aerobic anoxygenic phototrophic (AAP) bacteria harvest light energy using bacteriochlorophyll-containing reaction centers to supplement their mostly heterotrophic metabolism. While their abundance and growth have been intensively studied in coastal environments, much less is known about their activity in oligotrophic open ocean regions. Therefore, we combined in situ sampling in the North Pacific Subtropical Gyre, north of O'ahu island, Hawaii, with two manipulation experiments. Infra-red epifluorescence microscopy documented that AAP bacteria represented approximately 2% of total bacteria in the euphotic zone with the maximum abundance in the upper 50 m. They conducted active photosynthetic electron transport with maximum rates up to 50 electrons per reaction center per second. The in situ decline of bacteriochlorophyll concentration over the daylight period, an estimate of loss rates due to predation, indicated that the AAP bacteria in the upper 50 m of the water column turned over at rates of 0.75-0.90 d-1. This corresponded well with the specific growth rate determined in dilution experiments where AAP bacteria grew at a rate 1.05 ± 0.09 d-1. An amendment of inorganic nitrogen to obtain N:P = 32 resulted in a more than 10 times increase in AAP abundance over 6 days. The presented data document that AAP bacteria are an active part of the bacterioplankton community in the oligotrophic North Pacific Subtropical Gyre and that their growth was mostly controlled by nitrogen availability and grazing pressure.IMPORTANCEMarine bacteria represent a complex assembly of species with different physiology, metabolism, and substrate preferences. We focus on a specific functional group of marine bacteria called aerobic anoxygenic phototrophs. These photoheterotrophic organisms require organic carbon substrates for growth, but they can also supplement their metabolic needs with light energy captured by bacteriochlorophyll. These bacteria have been intensively studied in coastal regions, but rather less is known about their distribution, growth, and mortality in the oligotrophic open ocean. Therefore, we conducted a suite of measurements in the North Pacific Subtropical Gyre to determine the distribution of these organisms in the water column and their growth and mortality rates. A nutrient amendment experiment showed that aerobic anoxygenic phototrophs were limited by inorganic nitrogen. Despite this, they grew more rapidly than average heterotrophic bacteria, but their growth was balanced by intense grazing pressure.
Subject(s)
Bacteriochlorophylls , Phototrophic Processes , Bacteriochlorophylls/metabolism , Bacteria, Aerobic , Water/metabolism , Nitrogen/metabolism , Seawater/microbiologyABSTRACT
Dissolved inorganic nutrient concentrations in the surface waters (0 to 5 m) of the Northern Gulf of Mexico (NGoM) were analyzed from 1985 to 2019 (> 10,000 observations) to determine spatiotemporal trends and their connection to nutrients supplied from the Mississippi/Atchafalaya River (MAR). In the NGoM, annual mean dissolved inorganic P (DIP) concentrations increased significantly over time, while dissolved inorganic N (DIN) concentrations showed no temporal trend. With greater salinity, mean DIN:DIP decreased from above the Redfield ratio of 16 to below it, reflecting DIN losses and the more conservative behavior of DIP with salinity. Over the same time period, annual mean P (total dissolved P, DIP, dissolved organic P) loading from the MAR to the NGoM significantly increased, annual mean DIN and total dissolved N loading showed no temporal trend, and dissolved organic N loading significantly decreased. Though DIP increased in the MAR, MAR DIP alone was insufficient to explain the surface distribution of DIP with salinity. Therefore, increases in surface DIP in the NGoM are not simply a reflection of increasing MAR DIP, pointing to temporal changes in other DIP sources. The increase in NGoM DIP suggests greater N limitation for phytoplankton, with implications for N fixation and nutrient management.
ABSTRACT
Phago-mixotrophy, the combination of photoautotrophy and phagotrophy in mixoplankton, organisms that can combine both trophic strategies, have gained increasing attention over the past decade. It is now recognized that a substantial number of protistan plankton species engage in phago-mixotrophy to obtain nutrients for growth and reproduction under a range of environmental conditions. Unfortunately, our current understanding of mixoplankton in aquatic systems significantly lags behind our understanding of zooplankton and phytoplankton, limiting our ability to fully comprehend the role of mixoplankton (and phago-mixotrophy) in the plankton food web and biogeochemical cycling. Here, we put forward five research directions that we believe will lead to major advancement in the field: (i) evolution: understanding mixotrophy in the context of the evolutionary transition from phagotrophy to photoautotrophy; (ii) traits and trade-offs: identifying the key traits and trade-offs constraining mixotrophic metabolisms; (iii) biogeography: large-scale patterns of mixoplankton distribution; (iv) biogeochemistry and trophic transfer: understanding mixoplankton as conduits of nutrients and energy; and (v) in situ methods: improving the identification of in situ mixoplankton and their phago-mixotrophic activity.
ABSTRACT
Utilisation of dissolved organic phosphorus (DOP) by marine microbes as an alternative phosphorus (P) source when phosphate is scarce can help sustain non-Redfieldian carbon:nitrogen:phosphorus ratios and efficient ocean carbon export. However, global spatial patterns and rates of microbial DOP utilisation are poorly investigated. Alkaline phosphatase (AP) is an important enzyme group that facilitates the remineralisation of DOP to phosphate and thus its activity is a good proxy for DOP-utilisation, particularly in P-stressed regions. We present a Global Alkaline Phosphatase Activity Dataset (GAPAD) with 4083 measurements collected from 79 published manuscripts and one database. Measurements are organised into four groups based on substrate and further subdivided into seven size fractions based on filtration pore size. The dataset is globally distributed and covers major oceanic regions, with most measurements collected in the upper 20 m of low-latitude oceanic regions during summer since 1997. This dataset can help support future studies assessing global ocean P supply from DOP utilisation and provide a useful data reference for both field investigations and modelling activities.
ABSTRACT
The marine cyanobacterium Prochlorococcus can utilize glucose as a source of carbon. However, the relative importance of inorganic and organic carbon assimilation and the timing of glucose assimilation are still poorly understood in these numerically dominant cyanobacteria. Here, we investigated whole microbial community and group-specific primary production and glucose assimilation using incubations with radioisotopes combined with flow cytometry cell sorting. We also studied changes in the microbial community structure in response to glucose enrichments and analyzed the transcription of Prochlorocccus genes involved in carbon metabolism and photosynthesis. Our results showed a diel variation for glucose assimilation in Prochlorococcus, with maximum assimilation at midday and minimum at midnight (~2-fold change), which was different from that of the total microbial community. This suggests that the timing in glucose assimilation in Prochlorococcus is coupled to photosynthetic light reactions producing energy, it being more convenient for Prochlorococcus to show maximum glucose uptake precisely when the rest of microbial populations have their minimum glucose uptake. Many transcriptional responses to glucose enrichment occurred after 12- and 24-h periods, but community composition did not change. High-light Prochlorococcus strains were the most impacted by glucose addition, with transcript-level increases observed for genes in pathways for glucose metabolism, such as the pentose phosphate pathway, the Entner-Doudoroff pathway, glycolysis, respiration, and glucose transport. While Prochlorococcus C assimilation from glucose represented less than 0.1% of the bacterium's photosynthetic C fixation, increased assimilation during the day and glcH gene upregulation upon glucose enrichment indicate an important role of mixotrophic C assimilation by natural populations of Prochlorococcus. IMPORTANCE Several studies have demonstrated that Prochlorococcus, the most abundant photosynthetic organism on Earth, can assimilate organic molecules, such as amino acids, amino sugars, ATP, phosphonates, and dimethylsulfoniopropionate. This autotroph can also assimilate small amounts of glucose, supporting the hypothesis that Prochlorococcus is mixotrophic. Our results show, for the first time, a diel variability in glucose assimilation by natural populations of Prochlorococcus with maximum assimilation during midday. Based on our previous results, this indicates that Prochlorococcus could maximize glucose uptake by using ATP made during the light reactions of photosynthesis. Furthermore, Prochlorococcus showed a different timing of glucose assimilation from the total population, which may offer considerable fitness advantages over competitors "temporal niches." Finally, we observed transcriptional changes in some of the genes involved in carbon metabolism, suggesting that Prochlorococcus can use both pathways previously proposed in cyanobacteria to metabolize glucose.
Subject(s)
Organophosphonates , Prochlorococcus , Prochlorococcus/genetics , Prochlorococcus/metabolism , Glucose/metabolism , Seawater , Carbon/metabolism , Amino Acids/metabolism , Adenosine Triphosphate/metabolism , Amino Sugars/metabolismABSTRACT
Fossil hydrothermal systems on Mars are important exploration targets because they may have once been habitable and could still preserve evidence of microbial life. We investigated microbial communities within an active lava-induced hydrothermal system associated with the 2014-2015 eruption of Holuhraun in Iceland as a Mars analogue. In 2016, the microbial composition in the lava-heated water differed substantially from that of the glacial river and spring water sources that fed into the system. Several taxonomic and metabolic groups were confined to the water emerging from the lava and some showed the highest sequence similarities to subsurface ecosystems, including to the predicted thermophilic and deeply branching Candidatus Acetothermum autotrophicum. Measurements show that the communities were affected by temperature and other environmental factors. In particular, comparing glacial river water incubated in situ (5.7°C, control) with glacial water incubated within a lava-heated stream (17.5°C, warm) showed that microbial abundance, richness, and diversity increased in the warm treatment compared with the control, with the predicted major metabolism shifting from lithotrophy toward organotrophy and possibly phototrophy. In addition, thermophilic bacteria isolated from the lava-heated water and a nearby acidic hydrothermal system included the known endospore-formers Geobacillus stearothermophilus and Paenibacillus cisolokensis as well as a potentially novel taxon within the order Hyphomicrobiales. Similar lava-water interactions on Mars could therefore have generated habitable environments for microbial communities.
Subject(s)
Mars , Microbiota , Iceland , Temperature , WaterABSTRACT
Biogeographical classifications of the global ocean generalize spatiotemporal trends in species or biomass distributions across discrete ocean biomes or provinces. These classifications are generally based on a combination of remote-sensed proxies of phytoplankton biomass and global climatologies of biogeochemical or physical parameters. However, these approaches are limited in their capacity to account for subsurface variability in these parameters. The deployment of autonomous profiling floats in the Biogeochemical Argo network over the last decade has greatly increased global coverage of subsurface measurements of bio-optical proxies for phytoplankton biomass and physiology. In this study, we used empirical orthogonal function analysis to identify the main components of variability in a global data set of 422 annual time series of Chlorophyll a fluorescence and optical backscatter profiles. Applying cluster analysis to these results, we identified six biomes within the global ocean: two high-latitude biomes capturing summer bloom dynamics in the North Atlantic and Southern Ocean and four mid- and low-latitude biomes characterized by variability in the depth and frequency of deep chlorophyll maximum formation. We report the distribution of these biomes along with associated trends in biogeochemical and physicochemical environmental parameters. Our results demonstrate light and nutrients to explain most variability in phytoplankton distributions for all biomes, while highlighting a global inverse relationship between particle stocks in the euphotic zone and transfer efficiency into the mesopelagic zone. In addition to partitioning seasonal variability in vertical phytoplankton distributions at the global scale, our results provide a potentially novel biogeographical classification of the global ocean.
ABSTRACT
Considering the reported significant diazotrophic activities in open-ocean regions where primary production is strongly limited by phosphate, we explored the ability of diazotrophs to use other sources of phosphorus to alleviate the phosphate depletion. We tested the actual efficiency of the open-ocean, N2-fixer Crocosphaera watsonii to grow on organic phosphorus as the sole P source, and observed how the P source affects the cellular C, N, and P composition. We obtained equivalent growth efficiencies on AMP and DL-α-glycerophosphate as compared with identical cultures grown on phosphate, and survival of the population on phytic acid. Our results show that Crocosphaera cannot use all phosphomonoesters with the same efficiency, but it can grow without phosphate, provided that usable DOP and sufficient light energy are available. Also, results point out that organic phosphorus uptake is not proportional to alkaline phosphatase activity, demonstrating that the latter is not a suitable proxy to estimate DOP-based growth yields of organisms, whether in culture experiments or in the natural environment. The growth parameters obtained, as a function of the P source, will be critical to improve and calibrate mathematical models of diazotrophic growth and the distribution of nitrogen fixation in the global ocean.
ABSTRACT
The unicellular diazotrophic cyanobacterium Crocosphaera contributes significantly to fixed nitrogen inputs in the oligotrophic ocean. In the western tropical South Pacific Ocean (WTSP), these diazotrophs abound thanks to the phosphorus-rich waters provided by the South Equatorial Current, and iron provided aeolian and subsurface volcanic activity. East of the WTSP, the South Pacific Gyre (SPG) harbors the most oligotrophic and transparent waters of the world's oceans, where only heterotrophic diazotrophs have been reported before. Here, in the SPG, we detected unexpected accumulation of Crocosphaera at 50 m with peak abundances of 5.26 × 105 nifH gene copies l-1. The abundance of Crocosphaera at 50 m was in the same order of magnitude as those detected westwards in the WTSP and represented 100% of volumetric N2 fixation rates. This accumulation at 50 m was likely due to a deeper penetration of UV light in the clear waters of the SPG being detrimental for Crocosphaera growth and N2 fixation activity. Nutrient and trace metal addition experiments did not induce any significant changes in N2 fixation or Crocosphaera abundance, indicating that this population was not limited by the resources tested and could develop in high numbers despite the oligotrophic conditions. Our findings indicate that the distribution of Crocosphaera can extend into subtropical gyres and further understanding of their controlling factors is needed.
Subject(s)
Cyanobacteria , Seawater , Cyanobacteria/genetics , Nitrogen , Nitrogen Fixation/genetics , Pacific Ocean , Phosphorus , Seawater/microbiologyABSTRACT
Photosymbioses, intimate interactions between photosynthetic algal symbionts and heterotrophic hosts, are well known in invertebrate and protist systems. Vertebrate animals are an exception where photosynthetic microorganisms are not often considered part of the normal vertebrate microbiome, with a few exceptions in amphibian eggs. Here, we review the breadth of vertebrate diversity and explore where algae have taken hold in vertebrate fur, on vertebrate surfaces, in vertebrate tissues, and within vertebrate cells. We find that algae have myriad partnerships with vertebrate animals, from fishes to mammals, and that those symbioses range from apparent mutualisms to commensalisms to parasitisms. The exception in vertebrates, compared with other groups of eukaryotes, is that intracellular mutualisms and commensalisms with algae or other microbes are notably rare. We currently have no clear cell-in-cell (endosymbiotic) examples of a trophic mutualism in any vertebrate, while there is a broad diversity of such interactions in invertebrate animals and protists. This functional divergence in vertebrate symbioses may be related to vertebrate physiology or a byproduct of our adaptive immune system. Overall, we see that diverse algae are part of the vertebrate microbiome, broadly, with numerous symbiotic interactions occurring across all vertebrate and many algal clades. These interactions are being studied for their ecological, organismal, and cellular implications. This synthesis of vertebrate-algal associations may prove useful for the development of novel therapeutics: pairing algae with medical devices, tissue cultures, and artificial ecto- and endosymbioses.
Subject(s)
Plants , Symbiosis , Animals , Eukaryota/physiology , Mammals , Photosynthesis , Symbiosis/physiology , VertebratesABSTRACT
Dissolved organic phosphorus (DOP) is a critical nutritional resource for marine microbial communities. However, the relative bioavailability of different types of DOP, such as phosphomonoesters (P-O-C) and phosphoanhydrides (P-O-P), is poorly understood. Here we assess the utilization of these P sources by a representative bacterial copiotroph, Ruegeria pomeroyi DSS-3. All DOP sources supported equivalent growth by R. pomeroyi, and all DOP hydrolysis rates were upregulated under phosphorus depletion (-P). A long-chain polyphosphate (45polyP) showed the lowest hydrolysis rate of all DOP substrates tested, including tripolyphosphate (3polyP). Yet the upregulation of 45polyP hydrolysis under -P was greater than any other substrate analyzed. Proteomics revealed three common P acquisition enzymes potentially involved in polyphosphate utilization, including two alkaline phosphatases, PhoD and PhoX, and one 5'-nucleotidase (5'-NT). Results from DOP substrate competition experiments show that these enzymes likely have broad substrate specificities, including chain length-dependent reactivity toward polyphosphate. These results confirm that DOP, including polyP, are bioavailable nutritional P sources for R. pomeroyi, and possibly other marine heterotrophic bacteria. Furthermore, the chain-length dependent mechanisms, rates and regulation of polyP hydrolysis suggest that these processes may influence the composition of DOP and the overall recycling of nutrients within marine dissolved organic matter.
Subject(s)
Dissolved Organic Matter , Rhodobacteraceae , Phosphorus/metabolism , Polyphosphates/metabolism , Rhodobacteraceae/metabolismABSTRACT
Small pigmented eukaryotes (⩽ 5 µm) are an important, but overlooked component of global marine phytoplankton. The Amazon River plume delivers nutrients into the oligotrophic western tropical North Atlantic, shades the deeper waters, and drives the structure of microphytoplankton (> 20 µm) communities. For small pigmented eukaryotes, however, diversity and distribution in the region remain unknown, despite their significant contribution to open ocean primary production and other biogeochemical processes. To investigate how habitats created by the Amazon river plume shape small pigmented eukaryote communities, we used high-throughput sequencing of the 18S ribosomal RNA genes from up to five distinct small pigmented eukaryote cell populations, identified and sorted by flow cytometry. Small pigmented eukaryotes dominated small phytoplankton biomass across all habitat types, but the population abundances varied among stations resulting in a random distribution. Small pigmented eukaryote communities were consistently dominated by Chloropicophyceae (0.8-2 µm) and Bacillariophyceae (0.8-3.5 µm), accompanied by MOCH-5 at the surface or by Dinophyceae at the chlorophyll maximum. Taxonomic composition only displayed differences in the old plume core and at one of the plume margin stations. Such results reflect the dynamic interactions of the plume and offshore oceanic waters and suggest that the resident small pigmented eukaryote diversity was not strongly affected by habitat types at this time of the year.
Subject(s)
Chlorophyll/metabolism , Ecosystem , Phytoplankton/physiology , Rivers/chemistry , Seasons , Seawater/analysis , Chlorophyta/physiology , Diatoms/physiology , Dinoflagellida/physiologyABSTRACT
While algal phago-mixotrophs play a major role in aquatic microbial food webs, their diversity remains poorly understood. Recent studies have indicated several species of prasinophytes, early diverging green algae, to be able to consume bacteria for nutrition. To further explore the occurrence of phago-mixotrophy in green algae, we conducted feeding experiments with live fluorescently labeled bacteria stained with CellTracker Green CMFDA, heat-killed bacteria stained with 5-(4,6-dichlorotriazin-2-yl) aminofluorescein (DTAF), and magnetic beads. Feeding was detected via microscopy and/or flow cytometry in five strains of prasinophytes when provided with live bacteria: Pterosperma cristatum NIES626, Pyramimonas parkeae CCMP726, Pyramimonas parkeae NIES254, Nephroselmis pyriformis RCC618, and Dolichomastix tenuilepis CCMP3274. No feeding was detected when heat-killed bacteria or magnetic beads were provided, suggesting a strong preference for live prey in the strains tested. In parallel to experimental assays, green algal bacterivory was investigated using a gene-based prediction model. The predictions agreed with the experimental results and suggested bacterivory potential in additional green algae. Our observations underline the likelihood of widespread occurrence of phago-mixotrophy among green algae, while additionally highlighting potential biases introduced when using prey proxy to evaluate bacterial ingestion by algal cells.
Subject(s)
Chlorophyta , Bacteria/genetics , Computer Simulation , Food ChainABSTRACT
The unique symbiosis between a vertebrate salamander, Ambystoma maculatum, and unicellular green alga, Oophila amblystomatis, involves multiple modes of interaction. These include an ectosymbiotic interaction where the alga colonizes the egg capsule, and an intracellular interaction where the alga enters tissues and cells of the salamander. One common interaction in mutualist photosymbioses is the transfer of photosynthate from the algal symbiont to the host animal. In the A. maculatum-O. amblystomatis interaction, there is conflicting evidence regarding whether the algae in the egg capsule transfer chemical energy captured during photosynthesis to the developing salamander embryo. In experiments where we took care to separate the carbon fixation contributions of the salamander embryo and algal symbionts, we show that inorganic carbon fixed by A. maculatum embryos reaches 2% of the inorganic carbon fixed by O. amblystomatis algae within an egg capsule after 2 h in the light. After 2 h in the dark, inorganic carbon fixed by A. maculatum embryos is 800% of the carbon fixed by O. amblystomatis algae within an egg capsule. Using photosynthesis inhibitors, we show that A. maculatum embryos and O. amblystomatis algae compete for available inorganic carbon within the egg capsule environment. Our results confirm earlier studies suggesting a role of heterotrophic carbon fixation during vertebrate embryonic development. Our results also show that the considerable capacity of developing A. maculatum embryos for inorganic carbon fixation precludes our ability to distinguish any minor role of photosynthetically transferred carbon from algal symbionts to host salamanders using bicarbonate introduced to the egg system as a marker.
ABSTRACT
Mixotrophy, the combination of heterotrophic and autotrophic nutrition modes, is emerging as the rule rather than the exception in marine photosynthetic plankton. Trichodesmium, a prominent diazotroph ubiquitous in the (sub)tropical oceans, is generally considered to obtain energy via autotrophy. While the ability of Trichodesmium to use dissolved organic phosphorus when deprived of inorganic phosphorus sources is well known, the extent to which this important cyanobacterium may benefit from other dissolved organic matter (DOM) resources is unknown. Here we provide evidence of carbon-, nitrogen- and phosphorus-rich DOM molecules enhancing N2 fixation rates and nifH gene expression in natural Trichodesmium colonies collected at two stations in the western tropical South Pacific. Sampling at a third station located in the oligotrophic South Pacific Gyre revealed no Trichodesmium but showed presence of UCYN-B, although no nifH expression was detected. Our results suggest that Trichodesmium behaves mixotrophically in response to certain environmental conditions, providing them with metabolic plasticity and adding up to the view that mixotrophy is widespread among marine microbes.
Subject(s)
Nitrogen Fixation/drug effects , Organic Chemicals/pharmacology , Oxidoreductases/genetics , Trichodesmium/drug effects , Carbon/analysis , Carbon/pharmacology , Gene Expression Regulation, Bacterial/drug effects , Nitrogen/analysis , Nitrogen/pharmacology , Organic Chemicals/analysis , Pacific Ocean , Phosphorus/analysis , Phosphorus/pharmacology , Seawater/chemistry , Seawater/microbiology , Trichodesmium/genetics , Trichodesmium/metabolismABSTRACT
Bacteria living in the oligotrophic open ocean have various ways to survive under the pressure of nutrient limitation. Copepods, an abundant portion of the mesozooplankton, release nutrients through excretion and sloppy feeding that can support growth of surrounding bacteria. We conducted incubation experiments in the North Atlantic Subtropical Gyre to investigate the response of bacterial communities in the presence of copepods. Bacterial community composition and abundance measurements indicate that copepods have the potential to influence the microbial communities surrounding and associating with them - their 'zoosphere', in two ways. First, copepods may attract and support the growth of copiotrophic bacteria including representatives of Vibrionaceae, Oceanospirillales and Rhodobacteraceae in waters surrounding them. Second, copepods appear to grow specific groups of bacteria in or on the copepod body, particularly Flavobacteriaceae and Pseudoalteromonadaceae, effectively 'farming' them and subsequently releasing them. These distinct mechanisms provide a new view into how copepods may shape microbial communities in the open ocean. Microbial processes in the copepod zoosphere may influence estimates of oceanic bacterial biomass and in part control bacterial community composition and distribution in seawater.
Subject(s)
Bacteria/growth & development , Copepoda/physiology , Microbiota , Seawater/microbiology , Animals , Gammaproteobacteria , Nutrients/metabolism , Oceans and SeasABSTRACT
Polyphosphates and phosphomonoesters are dominant components of marine dissolved organic phosphorus (DOP). Collectively, DOP represents an important nutritional phosphorus (P) source for phytoplankton growth in the ocean, but the contribution of specific DOP sources to microbial community P demand is not fully understood. In a prior study, it was reported that inorganic polyphosphate was not bioavailable to the model diatoms Thalassiosira weissflogii and Thalassiosira pseudonana. However, in this study, we show that the previous finding was a misinterpretation based on a technical artefact of media preparation and that inorganic polyphosphate is actually widely bioavailable to Thalassiosira spp. In fact, orthophosphate, inorganic tripolyphosphate (3polyP), adenosine triphosphate (ATP) and adenosine monophosphate supported equivalent growth rates and final growth yields within each of four strains of Thalassiosira spp. However, enzyme activity assays revealed in all cultures that cell-associated hydrolysis rates of 3polyP were typically more than ~10-fold higher than degradation of ATP and the model phosphomonoester compound 4-methylumbelliferyl phosphate. These results build on prior work, which showed the preferential utilization of polyphosphates in the cell-free exudates of Thalassiosira spp., and suggest that inorganic polyphosphates may be a key bioavailable source of P for marine phytoplankton.