scholarly journals Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy

Author(s):  
Frank Xavier Ferrer-González ◽  
Brittany Widner ◽  
Nicole R. Holderman ◽  
John Glushka ◽  
Arthur S. Edison ◽  
...  

Abstract The communities of bacteria that assemble around marine microphytoplankton are predictably dominated by Rhodobacterales, Flavobacteriales, and families within the Gammaproteobacteria. Yet whether this consistent ecological pattern reflects the result of resource-based niche partitioning or resource competition requires better knowledge of the metabolites linking microbial autotrophs and heterotrophs in the surface ocean. We characterized molecules targeted for uptake by three heterotrophic bacteria individually co-cultured with a marine diatom using two strategies that vetted the exometabolite pool for biological relevance by means of bacterial activity assays: expression of diagnostic genes and net drawdown of exometabolites, the latter detected with mass spectrometry and nuclear magnetic resonance using novel sample preparation approaches. Of the more than 36 organic molecules with evidence of bacterial uptake, 53% contained nitrogen (including nucleosides and amino acids), 11% were organic sulfur compounds (including dihydroxypropanesulfonate and dimethysulfoniopropionate), and 28% were components of polysaccharides (including chrysolaminarin, chitin, and alginate). Overlap in phytoplankton-derived metabolite use by bacteria in the absence of competition was low, and only guanosine, proline, and N-acetyl-d-glucosamine were predicted to be used by all three. Exometabolite uptake pattern points to a key role for ecological resource partitioning in the assembly marine bacterial communities transforming recent photosynthate.

2020 ◽  
Author(s):  
Mario Uchimiya ◽  
William Schroer ◽  
Malin Olofsson ◽  
Arthur S. Edison ◽  
Mary Ann Moran

AbstractOrganic carbon transfer between photoautotrophic and heterotrophic microbes in the surface ocean mediated through metabolites dissolved in seawater is a central but poorly understood process in the global carbon cycle. In a synthetic microbial community in which diatom extracellular release of organic molecules sustained growth of a co-cultured bacterium, metabolite transfer was assessed over two diel cycles based on per cell quantification of phytoplankton endometabolites and bacterial transcripts. Of 31 phytoplankton endometabolites identified and classified into temporal abundance patterns, eight could be matched to patterns of bacterial transcripts mediating their uptake and catabolism. A model simulating the coupled endometabolite-transcription relationships hypothesized that one category of outcomes required an increase in phytoplankton metabolite synthesis in response to the presence of the bacterium. An experimental test of this hypothesis confirmed higher endometabolome accumulation in the presence of bacteria for all five compounds assigned to this category – leucine, glycerol-3-phosphate, glucose, and the organic sulfur compounds dihydroxypropanesulfonate and dimethylsulfoniopropionate. Partitioning of photosynthate into rapidly-cycling dissolved organic molecules at the expense of phytoplankton biomass production has implications for carbon sequestration in the deep ocean. That heterotrophic bacteria can impact this partitioning suggests a previously unrecognized influence on the ocean’s carbon reservoirs.Significance StatementMicrobes living in the surface ocean are critical players in the global carbon cycle, carrying out a particularly key role in the flux of carbon between the ocean and atmosphere. The release of metabolites by marine phytoplankton and their uptake by heterotrophic bacteria is one of the major routes of microbial carbon turnover. Yet the identity of these metabolites, their concentration in seawater, and the factors that affect their synthesis and release are poorly known. Here we provide experimental evidence that marine heterotrophic bacteria can affect phytoplankton production and extracellular release of metabolites. This microbial interaction has relevance for the partitioning of photosynthate between dissolved and particulate carbon reservoirs in the ocean, an important factor in oceanic carbon sequestration.


2017 ◽  
Vol 5 (18) ◽  
Author(s):  
Nathan S. Garcia ◽  
Cheuk-Man Yung ◽  
Katherine M. Davis ◽  
Tatiana Rynearson ◽  
Dana E. Hunt

ABSTRACT Phytoplankton often both provision and depend on heterotrophic bacteria. In order to investigate these relationships further, we sequenced draft genomes of three bacterial isolates from cultures of the marine diatom Thalassiosira rotula to identify metabolic functions that may support interactions with T. rotula.


2015 ◽  
Vol 112 (17) ◽  
pp. E2182-E2190 ◽  
Author(s):  
Harriet Alexander ◽  
Bethany D. Jenkins ◽  
Tatiana A. Rynearson ◽  
Sonya T. Dyhrman

Diverse communities of marine phytoplankton carry out half of global primary production. The vast diversity of the phytoplankton has long perplexed ecologists because these organisms coexist in an isotropic environment while competing for the same basic resources (e.g., inorganic nutrients). Differential niche partitioning of resources is one hypothesis to explain this “paradox of the plankton,” but it is difficult to quantify and track variation in phytoplankton metabolism in situ. Here, we use quantitative metatranscriptome analyses to examine pathways of nitrogen (N) and phosphorus (P) metabolism in diatoms that cooccur regularly in an estuary on the east coast of the United States (Narragansett Bay). Expression of known N and P metabolic pathways varied between diatoms, indicating apparent differences in resource utilization capacity that may prevent direct competition. Nutrient amendment incubations skewed N/P ratios, elucidating nutrient-responsive patterns of expression and facilitating a quantitative comparison between diatoms. The resource-responsive (RR) gene sets deviated in composition from the metabolic profile of the organism, being enriched in genes associated with N and P metabolism. Expression of the RR gene set varied over time and differed significantly between diatoms, resulting in opposite transcriptional responses to the same environment. Apparent differences in metabolic capacity and the expression of that capacity in the environment suggest that diatom-specific resource partitioning was occurring in Narragansett Bay. This high-resolution approach highlights the molecular underpinnings of diatom resource utilization and how cooccurring diatoms adjust their cellular physiology to partition their niche space.


2020 ◽  
Author(s):  
Marianne Acker ◽  
Shane L. Hogle ◽  
Paul M. Berube ◽  
Thomas Hackl ◽  
Ramunas Stepanauskas ◽  
...  

AbstractPhosphonates, organic compounds with a C-P bond, constitute 20-25% of phosphorus in high molecular weight dissolved organic matter and are a significant phosphorus source for marine microbes. However, little is known about phosphonate sources, biological function, or biogeochemical cycling. Here, we determine the biogeographic distribution and prevalence of phosphonate biosynthesis potential using thousands of genomes and metagenomes from the upper 250 meters of the global ocean. Potential phosphonate producers are taxonomically diverse, occur in widely distributed and abundant marine lineages (including SAR11 and Prochlorococcus) and their abundance increases with depth. Within those lineages, phosphonate biosynthesis and catabolism pathways are mutually exclusive, indicating functional niche partitioning of organic phosphorus cycling in the marine microbiome. Surprisingly, one strain of Prochlorococcus (SB) can allocate more than 40% of its cellular P-quota towards phosphonate production. Chemical analyses and genomic evidence suggest that phosphonates in this strain are incorporated into surface layer glycoproteins that may act to reduce mortality from grazing or viral infection. Although phosphonate production is a low-frequency trait in Prochlorococcus populations (~ 5% of genomes), experimentally derived production rates suggest that Prochlorococcus could produce a significant fraction of the total phosphonate in the oligotrophic surface ocean. These results underscore the global biogeochemical impact of even relatively rare functional traits in abundant groups like Prochlorococcus and SAR11.


Sci ◽  
2020 ◽  
Vol 2 (2) ◽  
pp. 41
Author(s):  
Mark Burchell ◽  
Kathryn Harriss

A prime site of astrobiological interest within the Solar System is the interior ocean of Enceladus. This ocean has already been shown to contain organic molecules, and is thought to have the conditions necessary for more complex organic biomolecules to emerge and potentially even life itself. This sub-surface ocean has been accessed by Cassini, an unmanned spacecraft that interacted with the water plumes ejected naturally from Enceladus. The encounter speed with these plumes and their contents, was between 5 and 15 km s−1. Encounters at such speeds allow analysis of vapourised material from submicron-sized particles within the plume, but sampling micron-sized particles remains an open question. The latter particles can impact metal targets exposed on the exterior of future spacecraft, producing impact craters lined with impactor residue, which can then be analysed. Although there is considerable literature on how mineral grains behave in such high-speed impacts, and also on the relationship between the crater residue and the original grain composition, far less is known regarding the behaviour of organic particles. Here we consider a deceptively simple yet fundamental scientific question: for impacts at speeds of around 5–6 kms−1 would the impactor residue alone be sufficient to enable us to recognise the signature conferred by organic particles? Furthermore, would it be possible to identify the organic molecules involved, or at least distinguish between aromatic and aliphatic chemical structures? For polystyrene (aromatic-rich) and poly(methyl methacrylate) (solely aliphatic) latex particles impinging at around 5 km s−1 onto metal targets, we find that sufficient residue is retained at the impact site to permit identification of a carbon-rich projectile, but not of the particular molecules involved, nor is it currently possible to discriminate between aromatic-rich and solely aliphatic particles. This suggests that an alternative analytical method to simple impacts on metal targets is required to enable successful collection of organic samples in a fly-by Enceladus mission, or, alternatively, a lower encounter speed is required.


Sci ◽  
2020 ◽  
Vol 2 (1) ◽  
pp. 12
Author(s):  
Mark Burchell ◽  
Kathryn Harriss

A prime site of astrobiological interest within the Solar System is the interior ocean of Enceladus. This ocean has already been shown to contain organic molecules, and is thought to have the conditions necessary for more complex organic biomolecules to emerge and potentially even life itself. This sub-surface ocean has been accessed by Cassini, an unmanned spacecraft that interacted with the water plumes ejected naturally from Enceladus. The encounter speed with these plumes and their contents, was 5 km s−1 and above. Encounters at such speeds allow analysis of vapourised material from submicron-sized particles within the plume, but sampling micron-sized particles remains an open question. The latter particles can impact metal targets exposed on the exterior of future spacecraft, producing impact craters lined with impactor residue, which can then be analysed. Although there is considerable literature on how mineral grains behave in such high-speed impacts, and also on the relationship between the crater residue and the original grain composition, far less is known regarding the behaviour of organic particles. Here we consider a deceptively simple yet fundamental scientific question: for impacts at speeds of around 5−6 kms−1 would the impactor residue alone be sufficient to enable us to recognise the signature conferred by organic particles? Furthermore, would it be possible to identify the organic molecules involved, or at least distinguish between aromatic and aliphatic chemical structures? For polystyrene (aromatic-rich) and poly(methyl methacrylate) (solely aliphatic) latex particles impinging at around 5 km s-1 onto metal targets, we find that sufficient residue is retained at the impact site to permit identification of a carbon-rich projectile, but not of the particular molecules involved, nor is it currently possible to discriminate between aromatic-rich and solely aliphatic particles. This suggests that an alternative analytical method to simple impacts on metal targets is required to enable successful collection of organic samples in a fly-by Enceladus mission, or, alternatively, a lower encounter speed is required.


2016 ◽  
Vol 13 (2) ◽  
pp. 330 ◽  
Author(s):  
Cathleen Zindler-Schlundt ◽  
Hannah Lutterbeck ◽  
Sonja Endres ◽  
Hermann W. Bange

Environmental context Ocean acidification affects marine algae and bacteria, which can produce climate active trace gases such as methane or dimethylsulfide from marine dimethylsulfoxide. We conducted field experiments simulating future ocean acidification, and showed that dimethylsulfoxide concentrations decreased with increasing acidification. Less dimethylsulfoxide in the future can affect climate by influencing the concentration of methane and dimethylsulfide. Abstract Ongoing ocean acidification (OA), caused by continuous anthropogenic CO2 emissions, seems to decrease the concentrations of dimethylsulfide (DMS) and its precursor dimethylsulfoniopropionate (DMSP) in the surface oceans. This might have consequences for future climate due to changes in formation and growth of atmospheric sulfate aerosols formed from DMS. However, the effect of OA on dimethylsulfoxide (DMSO), another intermediate of the DMS pathway and a potential precursor of oceanic methane, is unknown. Therefore, we investigated the effect of OA on the DMSO concentrations in a mesocosm study conducted in a Norwegian fjord in spring 2011. Dissolved and particulate DMSO concentrations (DMSOd/p) decreased with pH during the course of the experiment. Temperature correlated inversely with DMSOd concentrations during the first week of the experiment, reflecting the influence of temperature dependent biological activities on DMSOd pathways. Furthermore, DMSOd increased with the cell abundance of heterotrophic bacteria, cryptophytes, and the cyanobacterium Synechococcus sp. Nitrate availability influenced the distribution of cryptophytes and Synechococcus sp. in the same way as DMSOd, indicating again a possible link between these phytoplankton taxa and DMSOd. We conclude that ongoing OA may lead to decreasing DMSO concentrations in the surface ocean that, in turn, might affect the oceanic distributions of DMS and methane.


2009 ◽  
Vol 66 (6) ◽  
pp. 1007-1018 ◽  
Author(s):  
Mara S. Zimmerman ◽  
Stephanie N. Schmidt ◽  
Charles C. Krueger ◽  
M. Jake Vander Zanden ◽  
Randy L. Eshenroder

Resource polymorphisms are widely observed in fishes; however, ontogenetic contributions to morphological and ecological differences are poorly understood. This study examined whether ontogenetic changes in niche partitioning could explain morphological and buoyancy differences between lake trout ( Salvelinus namaycush ) morphotypes in Great Slave Lake (Northwest Territories, Canada). Morphometric analysis, buoyancy, capture depth, diet, and stable isotope data were used in concert to determine whether (i) differences occur in small, as well as large, lake trout, (ii) ontogenetic changes in morphology and buoyancy correlate with shifts in depth or diet, and (iii) a subset of small trout, putatively identified as “humpers”, are distinct from other morphotypes. Ontogenetic changes in lake trout morphology were associated with an ecological shift between benthic and pelagic feeding. Resource partitioning between lean and siscowet-like trout occurred within benthic (small trout) and pelagic (large trout) habitats. The humper subset did not differ from small siscowet-like trout. By combining multiple methods and an ontogenetic perspective, our study provides novel perspectives on resource polymorphisms in large, deep lakes and on existing interpretations of stable isotope data from large lakes in general.


2012 ◽  
Vol 66 (12) ◽  
pp. 2556-2561 ◽  
Author(s):  
Tomonori Kindaichi ◽  
Shota Yuri ◽  
Noriatsu Ozaki ◽  
Akiyoshi Ohashi

The coexistence of uncultured heterotrophic bacteria belonging to the phylum Chloroflexi has often been observed in anaerobic ammonium oxidation (anammox) reactors fed with synthetic nutrient medium without organic carbon compounds. To determine if coexisting Chloroflexi in anammox reactors scavenge organic matter derived from anammox bacterial cells, the present study was conducted to investigate the substrate uptake pattern of the uncultured Chloroflexi present in an anammox reactor and to clarify if they take up microbial products derived from anammox bacterial cells. To accomplish this, combined microautoradiography and fluorescence in situ hybridization (MAR–FISH) was conducted. Phylogenetic analysis revealed that 36% of the clones analyzed in this study were affiliated with Chloroflexi. The sequence similarities to Anaerolinea thermophila and Caldilinea aerophila within the phylum Chloroflexi were only 81.0–88.7% and 80.3–83.8%, respectively. The uncultured Chloroflexi were found to incorporate sucrose, glucose, and N-acetyl-glucosamine. The 14C-tracing experiment revealed that the uncultured Chloroflexi were clearly MAR-positive, indicating the utilization of decaying anammox bacterial cell materials. Taken together, these results indicate that coexisting uncultured Chloroflexi in anammox reactors scavenge organic compounds derived from anammox bacterial cells.


Biologia ◽  
2015 ◽  
Vol 70 (1) ◽  
Author(s):  
Christoph Randler ◽  
Stefan Pentzold ◽  
Constanze Pentzold

AbstractDuring their staging at stopover sites, migrants compete with resident species over food resources. This ‘resource competition hypothesis’ has often been examined in breeding areas of songbirds, but little is known about resource competition between migrants and resident species at stopover sites. We studied foraging behaviour and microhabitat of the endemic resident species Cyprus Wheatear Oenanthe cypriaca in comparison to eleven migrating species of the same genus or of the same flycatching guild during spring migration on Cyprus, a Mediterranean stopover site. We characterized microhabitats of congeneric Oenanthe species by less cover overhead and low perches and distinguished them from migrating Ficedula hypoleuca, Ficedula albicollis and Phoenicurus phoenicurus, which preferred high cover overhead and medium perches. In a hierarchical cluster analysis, O. cypriaca clustered together with three shrike species Lanius and the flycatcher Muscicapa striata, with less cover overhead, but high perches. During foraging, hopping behaviour discriminated best among the Oenanthe species. Multidimensional scaling on foraging behaviour showed that O. cypriaca is clearly distinct from the other species. Direct competition (aggressive encounters) between the resident species and migrants was rarely observed. Our results provide support for niche partitioning and coexistence between migrants and a resident species at a stopover site.


Sign in / Sign up

Export Citation Format

Share Document