Undaria pinnatifida exudates trigger shifts in seawater chemistry and microbial communities from Atlantic Patagonian coasts

The invasive kelp Undaria pinnatifida has spread from northeastern Asia to temperate coastal environments worldwide, with profound effects on colonized ecosystems. In this work, we analyzed the effect of exudates from U. pinnatifida on the chemical and microbial properties of seawater from a semi-enclosed gulf from Atlantic Patagonia. Exudates of U. pinnatifida, consisting mainly of carbohydrates, were released at a rate of 1.6 ± 0.8 mg C g−1 algae day−1, affecting the quality and optical properties of seawater in experimental incubations. Parallel factor analysis based on excitation-emission matrices collected from exudates revealed the presence of two humic-like and one non-humic fluorescent components. Exudate release stimulated microbial growth and polysaccharide degrading activity in seawater. After a 7-day incubation of fresh seawater with the exudates, changes in microbial community structure were analyzed by large-scale 16S rRNA gene amplicon sequencing. Copiotrophic and fermentative genera such as Spirochaeta (Spirochaetes) and Propionigenium (Fusobacteria) increased in the incubations with algal exudates. Genomic potential prediction revealed that the selected bacterial community could have higher ribosome content - an indicator of the potential for reaching higher metabolic rates - and genes for the degradation of complex organic compounds such as polysaccharides and other carbohydrates present in the exudates. Nutrient addition triggered the emergence of other microbial populations with different ecophysiological niches: unclassified Flavobacteriales, unclassified bacteria related to the recently described Phylum Kiritimatiellaeota, as well as potential pathogens such as Vibrio (Gammaproteobacteria) and Arcobacter (Epsilonproteobacteria), suggesting potential synergistic effects between invasive macroalgae and human activities.

A multiomic analysis of in situ coral–turf algal interactions

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral–turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.

Fluorescent organic exudates of corals and algae in tropical reefs are compositionally distinct and increase with nutrient enrichment

Dissolved organic matter (DOM) composition is a key determinant of microbial community metabolism and trophic nutrient transfer. On coral reefs, four primary groups of benthic organisms dominate photosynthetic production: corals, macroalgae, microphytobenthos, and encrusting algae on rubble, all of which exude significant quantities of DOM. We conducted a mesocosm experiment to characterize and contrast DOM exudates from these four organismal groups under three levels of continuous inorganic nutrient enrichment. We measured bulk dissolved organic carbon and nitrogen and the multivariate spectral characteristics of fluorescent DOM (fDOM). Moderate nutrient enrichment enhanced DOM exudation by all producers. Corals exuded rapidly accumulating DOM with a markedly high concentration of aromatic amino acid-like fDOM components that clearly distinguishes them from algal exudates, which were dominated by humic-like fDOM components and did not accumulate significantly. Our results emphasize the differences between coral and algae in their potential to influence microbial communities and metabolism in reefs.

Fluorescent organic exudates of corals and algae in tropical reefs are compositionally distinct and increase with nutrient enrichment

Dissolved organic matter (DOM) composition is a key determinant of microbial community metabolism and trophic nutrient transfer. On coral reefs, four primary groups of benthic organisms dominate photosynthetic production: corals, macroalgae, microphytobenthos, and encrusting algae on rubble, all of which exude significant quantities of DOM. We conducted a mesocosm experiment to characterize and contrast DOM exudates from these four organismal groups under three levels of continuous inorganic nutrient enrichment. We measured bulk dissolved organic carbon and nitrogen and the multivariate spectral characteristics of fluorescent DOM (fDOM). Moderate nutrient enrichment enhanced DOM exudation by all producers. Corals exuded rapidly accumulating DOM with a markedly high concentration of aromatic amino acid-like fDOM components that clearly distinguishes them from algal exudates, which were dominated by humic-like fDOM components and did not accumulate significantly. Our results emphasize the differences between coral and algae in their potential to influence microbial communities and metabolism in reefs.

Molecular insights into the microbial formation of marine dissolved organic matter: recalcitrant or labile?

The degradation of marine dissolved organic matter (DOM) is an important control variable in the global carbon cycle. For our understanding of the kinetics of organic matter cycling in the ocean, it is crucial to achieve a mechanistic and molecular understanding of its transformation processes. A long-term microbial experiment was performed to follow the production of non-labile DOM by marine bacteria. Two different glucose concentrations and dissolved algal exudates were used as substrates. We monitored the bacterial abundance, concentrations of dissolved and particulate organic carbon (DOC, POC), nutrients, amino acids and transparent exopolymer particles (TEP) for 2 years. The molecular characterization of extracted DOM was performed by ultrahigh resolution Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS) after 70 days and after ∼2 years of incubation. Although glucose quickly degraded, a non-labile DOC background (5–9% of the initial DOC) was generated in the glucose incubations. Only 20% of the organic carbon from the algal exudate degraded within the 2 years of incubation. The degradation rates for the non-labile DOC background in the different treatments varied between 1 and 11 μmol DOC L−1 year−1. Transparent exopolymer particles, which are released by microorganisms, were produced during glucose degradation but decreased back to half of the maximum concentration within less than 3 weeks (degradation rate: 25 μg xanthan gum equivalents L−1 d−1) and were below detection in all treatments after 2 years. Additional glucose was added after 2 years to test whether labile substrate can promote the degradation of background DOC (co-metabolism; priming effect). A priming effect was not observed but the glucose addition led to a slight increase of background DOC. The molecular analysis demonstrated that DOM generated during glucose degradation differed appreciably from DOM transformed during the degradation of the algal exudates. Our results led to several conclusions: (i) based on our experimental setup, higher substrate concentration resulted in a higher concentration of non-labile DOC; (ii) TEP, generated by bacteria, degrade rapidly, thus limiting their potential contribution to carbon sequestration; (iii) the molecular signatures of DOM derived from algal exudates and glucose after 70 days of incubation differed strongly from refractory DOM. After 2 years, however, the molecular patterns of DOM in glucose incubations were more similar to deep ocean DOM whereas the degraded exudate was still different.

Molecular insights into the microbial formation of marine dissolved organic matter: recalcitrant or labile?

The degradation of marine dissolved organic matter (DOM) is an important control variable in the global carbon cycle and dependent on the DOM composition. For our understanding of the kinetics of organic matter cycling in the ocean, it is therefore crucial to achieve a mechanistic and molecular understanding of its transformation processes. A long-term microbial experiment was performed to follow the production of non-labile DOM by marine bacteria. Two different glucose concentrations and dissolved algal exudates were used as substrates. We monitored the bacterial abundance, concentrations of dissolved and particulate organic carbon (DOC, POC), nutrients, amino acids, and transparent exopolymer particles (TEP) for two years. Ultrahigh resolution Fourier Transform Ion Cyclotron Resonance Mass Spectrometry (FT-ICR-MS) allowed the molecular characterization of extracted DOM after 70 days and after ∼2 years of incubation. Although glucose was quickly degraded, a DOC background was generated in glucose incubations. Only 20% of the organic carbon from algal exudate was degraded within the 2 years of incubation. TEP, which are released by micro-organisms, were produced during glucose degradation but decreased within less than three weeks back to half of the maximum concentration and were below detection in all treatments after 2 years. The molecular analysis demonstrated that DOM generated during glucose degradation differed appreciably from DOM produced during the degradation of the algal exudates. Our results led to several conclusions: (i) Higher substrate levels result in a higher level of non-labile DOC which is an important prerequisite for carbon sequestration in the ocean; (ii) TEP are generated by bacteria but are also degraded rapidly, thus limiting their potential contribution to carbon sequestration; (iii) The molecular signatures of DOM derived from algal exudates or glucose after 70 days of incubation differed strongly from refractory DOM. After 2 years, however, the molecular patterns of DOM in glucose incubations were more similar to deep ocean DOM whereas the degraded exudate was still different.

The role of iron species on the competition of two coastal diatoms, <i>Skeletonema costatum</i> and <i>Thalassosira weissflogii</i>

Coastal diatoms are often exposed to macronutrient (N and P) and Fe enrichment. However, how these exposures influence on Fe biogeochemical cycle and then on diatom interspecific competition is unknown. In this study, two non-toxic coastal diatoms, Skeletonema costatum and Thalassosira weissflogii were exposed to N, P, and Fe enrichment for four-day. The growth of algae was co-controlled by macronutrient and Fe species (Fe (III)-EDTA, Fe(OH)3, dissolved, colloidal, and particulate Fe from culture medium). The influence of Fe species on algal cell density was more significant than macronutrient. When S. costatum coexisted with T. weissflogii, their cell density ratios were ranged between 5.57–7.03 times, indicating that S. costatum was more competitive than T. weissflogii. There were not significant correlation between cell density ratio and iron requirement, including iron adsorption and absorption per cell, iron adsorption and absorption by all algal cells. As Fe complexing ligands, algal exudates can promote diatom growth itself and such promotion on S. costatum was more obvious than that on T. weissflogii. Iron species was a key determinant on interspecific competition of coastal diatom, and the degree of bioavailability was described as follows: dissolved iron from own exudates > colloidal iron from own exudates > particulate iron from own exudates > particulate iron from another algal exudates > colloidal iron from another algal exudates > dissolved iron from another algal exudates > Fe (III)-EDTA> Fe (OH)3.