Dissolved free amino acids, combined amino acids, and DNA as sources of carbon and nitrogen to marine bacteria

Jørgensen, Niels O. G.; Kroer, Niels; Coffin, RB; Yang, Xihua; Lee, C.

doi:10.3354/meps098135

Cited by 147 publications

(136 citation statements)

References 19 publications

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“…Our sediment pore water analyses show that ambient inorganic nitrogen concentrations are comparatively low in the direct vicinity of C. orbicularis (that is, within a radius of 20 cm from the animals), suggesting that diazotrophy is of particular advantage for the bacterial symbiont in this habitat. In marine systems, the main sources of nitrogen available for bacterial growth (besides N 2 ) are NH 4 + and free amino acids 34 , as well asto a lesser extent-NO 3 − , NO 2 − and urea 35 . In seagrass bed sediments in particular, NH 4 + is considered to be the dominating nitrogen source, with concentrations of up to 175 µM in some areas 36 .…”

Section: Resultsmentioning

confidence: 99%

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

et al. 2016

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The shallow water bivalve Codakia orbicularis lives in symbiotic association with a sulfur-oxidizing bacterium in its gills. The endosymbiont fixes CO 2 and thus generates organic carbon compounds, which support the host's growth. To investigate the uncultured symbiont's metabolism and symbiont-host interactions in detail we conducted a proteogenomic analysis of purified bacteria. Unexpectedly, our results reveal a hitherto completely unrecognized feature of the C. orbicularis symbiont's physiology: the symbiont's genome encodes all proteins necessary for biological nitrogen fixation (diazotrophy). Expression of the respective genes under standard ambient conditions was confirmed by proteomics. Nitrogenase activity in the symbiont was also verified by enzyme activity assays. Phylogenetic analysis of the bacterial nitrogenase reductase NifH revealed the symbiont's close relationship to free-living nitrogen-fixing Proteobacteria from the seagrass sediment. The C. orbicularis symbiont, here tentatively named 'Candidatus Thiodiazotropha endolucinida', may thus not only sustain the bivalve's carbon demands. C. orbicularis may also benefit from a steady supply of fixed nitrogen from its symbiont-a scenario that is unprecedented in comparable chemoautotrophic symbioses. Mutualistic associations between marine invertebrates and sulfur-oxidizing (thiotrophic) bacteria are a well-documented and widespread phenomenon in a variety of sulfidic habitats ranging from hydrothermal vents to shallow-water coastal ecosystems 1-3 . Thioautotrophic symbionts generate energy through sulfide oxidation and provide their hosts with organic carbon. In the Lucinidae, a diverse family of marine bivalves, all members are obligatorily dependent on their bacterial gill endosymbionts after larval development and metamorphosis 4 . The shallowwater lucinid Codakia orbicularis, which lives in the sediment beneath the tropical seagrass Thalassia testudinum along the Caribbean and Western Atlantic coast 5 , harbours a single species of endosymbionts in its gills 6 . The symbiont has been shown to be newly acquired by each clam generation 7,8 from a pool of freeliving symbiosis-competent bacteria in the environment 9 , rather than being inherited from clam parents. C. orbicularis appears not to release its endosymbionts, even under adverse conditions, but can digest them as a source of nutrition [10][11][12] . Moreover, bacterial cell division seems to be inhibited inside the host tissue. The majority of the symbiont population was shown to be polyploid (that is, containing multiple genome copies), while dividing symbiont cell stages are very rarely observed in host bacteriocytes 13 . The host undoubtedly benefits from the symbiont both by way of detoxification of its sulfidic environment and by supply of organic compounds through the bacterial Calvin-Benson cycle. It remains questionable, however, whether the symbiont gains any advantage from this association in evolutionary terms 11 .Biological nitrogen fixation (diazotrophy) is the conversion of ...

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Section: Resultsmentioning

confidence: 99%

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

et al. 2016

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“…Proteins and peptides represent a major component of all living cells and have also been identified as major substrates for heterotrophic microorganisms in fresh waters (Kirchman et al, 1985;Rosenstock and Simon, 1993;Jørgensen et al, 1993;Tranvik and Jørgensen, 1995). A recent review by Kirchman (2003) concludes that amino acids typically sustain more than 20% of the bacterial carbon demand in a wide range of habitats (lakes, estuarine and marine), but the variation between and within these habitats can be large (from 6% to all of the carbon demand for lake bacterioplankton).…”

Section: Discussionmentioning

confidence: 99%

“…DFAA were analyzed by high-performance liquid chromatography (HPLC) and detected as fluorescent primary amines after derivatization with o-phthaldialdehyde (OPA) according to Lindroth and Mopper (1979) with modifications according to Jørgensen et al (1993). For the derivatization, a 20 ml water sample was mixed with 4 ml OPA solution in a Waters Alliance 2695 HPLC module and was allowed to react for 1 min before injection and separation on a 3.9 Â 150 mm Nova-Pak C18 steel column (Waters Corporation, Milford, MA, USA).…”

Section: Sample Collectionmentioning

confidence: 99%

Links between bacterial production, amino-acid utilization and community composition in productive lakes

et al. 2007

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Influence of distribution and abundance of bacterial taxa on ecosystem function are poorly understood for natural microbial communities. We related 16S rRNA-based terminal restriction fragment length polymorphism to bacterial production and arginine uptake kinetics to test if functional features of bacterioplankton in four lakes could be predicted from community composition. Maximum arginine uptake rate (arginine V max ) ranged from 10% to 100% of bacterial production. Owing to high growth efficiencies on arginine (63-77%), the bacterial community could potentially saturate its carbon demand using this single organic substrate, for example, during sudden surges of free amino acids. However, due to low in situ concentrations of arginine in these lakes (o0.9 lg l À1 ), actual uptake rates at ambient concentrations rarely exceeded 10% of V max . Bacterial production and arginine V max could be predicted from a subset of bacterial ribotypes, tentatively affiliated with several bacterial divisions (Cyanobacteria, Actinobacteria, Bacteroidetes and Proteobacteria). Multivariate statistical analysis indicates that there were both highly important and less important ribotypes for the prediction of bacterial production and arginine V max . These populations were either negatively or positively related to the respective functional feature, indicating contrasting ecological roles. Our study provides a statistically robust demonstration that, apart from environmental conditions, patterns in bacterial community composition can also be used to predict lake ecosystem function.

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“…The growth rate in the Phe treatment was higher than the growth rates in all other dissolved nitrogen treatments as well as that in the control treatment. However, growth rates did not differ between the (NH 4 ) 2 SO 4 , KNO 3 , and GlcNAc treatments and the control, and was lower in the NH 4 NO 3 treatment compared with the control. …”

Section: (C) Supporting Experimentsmentioning

confidence: 77%

“…Prokaryotes such as bacteria, cyanobacteria, and archaea absorb DON directly from environmental water to increase their populations [2][3][4]. The DON absorbed by prokaryotes is believed to be transported indirectly to aquatic animals at higher trophic levels via the food chain for use as a nutrient source.…”

Section: Introductionmentioning

confidence: 99%

An aquatic vertebrate can use amino acids from environmental water

2016

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Conventional food-web theory assumes that nutrients from dissolved organic matter are transferred to aquatic vertebrates via long nutrient pathways involving multiple eukaryotic species as intermediary nutrient transporters. Here, using larvae of the salamander Hynobius retardatus as a model system, we provide experimental evidence of a shortcut nutrient pathway by showing that H. retardatus larvae can use dissolved amino acids for their growth without eukaryotic mediation. First, to explore which amino acids can promote larval growth, we kept individual salamander larvae in one of eight different high-concentration amino acid solutions, or in control water from which all other eukaryotic organisms had been removed. We thus identified five amino acids (lysine, threonine, serine, phenylalanine, and tyrosine) as having the potential to promote larval growth. Next, using 15 N-labelled amino acid solutions, we demonstrated that nitrogen from dissolved amino acids was found in larval tissues. These results suggest that salamander larvae can take up dissolved amino acids from environmental water to use as an energy source or a growth-promoting factor. Thus, aquatic vertebrates as well as aquatic invertebrates may be able to use dissolved organic matter as a nutrient source.

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Dissolved free amino acids, combined amino acids, and DNA as sources of carbon and nitrogen to marine bacteria

Cited by 147 publications

References 19 publications

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

Links between bacterial production, amino-acid utilization and community composition in productive lakes

An aquatic vertebrate can use amino acids from environmental water

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