Abstract:Trichodesmium is a marine, diazotrophic cyanobacterium that plays a central role in the biogeochemical cycling of carbon and nitrogen. Colonies ubiquitously co‐occur with a diverse microbiome of heterotrophic bacteria. We show that manipulation of the microbiome with quorum sensing acyl homoserine lactones (AHLs) significantly modulated rates of N2 fixation by Trichodesmium collected from the western North Atlantic, with positive and negative effects of varied magnitude. Changes in Trichodesmium N2 fixation di… Show more
“…Our study is unique among the many genomic-based attempts to untangle the complex Trichodesmium -bacteria interactions, because it provides direct experimental evidence for the actual components of dust-Fe acquisition by the consortium. We confirmed genomic predictions of siderophore production and uptake by the consortium members 26 and support the concept that Trichodesmium and its colony microbes act as a synchronized metabolic circuit sharing key resources 13 . Our study adds to a growing body of research indicating that interspecies interactions control cycling of nutrients, such as nitrogen, carbon, phosphorus, iron, and vitamin B 12 37,38 .…”
Section: Discussionsupporting
confidence: 78%
“…Colonies of Trichodesmium host many associated bacteria which are distinct from free-living bacteria in seawater 10–12 . Trichodesmium and its associated bacteria exchange nutrients and organic molecules between them and act together to optimize the growth of the whole consortium 13,14 .Fig. 1Cartoon representation of the proposed dust-bound Fe acquisition pathway employed mutually by Trichodesmium colonies and associated bacteria.…”
Iron (Fe) bioavailability limits phytoplankton growth in vast ocean regions. Iron-rich dust uplifted from deserts is transported in the atmosphere and deposited on the ocean surface. However, this dust is a poor source of iron for most phytoplankton since dust-bound Fe is poorly soluble in seawater and dust rapidly sinks out of the photic zone. An exception is
Trichodesmium
, a globally important, N
2
fixing, colony forming, cyanobacterium, which efficiently captures and shuffles dust to its colony core.
Trichodesmium
and bacteria that reside within its colonies carry out diverse metabolic interactions. Here we show evidence for mutualistic interactions between
Trichodesmium
and associated bacteria for utilization of iron from dust, where bacteria promote dust dissolution by producing Fe-complexing molecules (siderophores) and
Trichodesmium
provides dust and optimal physical settings for dissolution and uptake. Our results demonstrate how intricate relationships between producers and consumers can influence productivity in the nutrient starved open ocean.
“…Our study is unique among the many genomic-based attempts to untangle the complex Trichodesmium -bacteria interactions, because it provides direct experimental evidence for the actual components of dust-Fe acquisition by the consortium. We confirmed genomic predictions of siderophore production and uptake by the consortium members 26 and support the concept that Trichodesmium and its colony microbes act as a synchronized metabolic circuit sharing key resources 13 . Our study adds to a growing body of research indicating that interspecies interactions control cycling of nutrients, such as nitrogen, carbon, phosphorus, iron, and vitamin B 12 37,38 .…”
Section: Discussionsupporting
confidence: 78%
“…Colonies of Trichodesmium host many associated bacteria which are distinct from free-living bacteria in seawater 10–12 . Trichodesmium and its associated bacteria exchange nutrients and organic molecules between them and act together to optimize the growth of the whole consortium 13,14 .Fig. 1Cartoon representation of the proposed dust-bound Fe acquisition pathway employed mutually by Trichodesmium colonies and associated bacteria.…”
Iron (Fe) bioavailability limits phytoplankton growth in vast ocean regions. Iron-rich dust uplifted from deserts is transported in the atmosphere and deposited on the ocean surface. However, this dust is a poor source of iron for most phytoplankton since dust-bound Fe is poorly soluble in seawater and dust rapidly sinks out of the photic zone. An exception is
Trichodesmium
, a globally important, N
2
fixing, colony forming, cyanobacterium, which efficiently captures and shuffles dust to its colony core.
Trichodesmium
and bacteria that reside within its colonies carry out diverse metabolic interactions. Here we show evidence for mutualistic interactions between
Trichodesmium
and associated bacteria for utilization of iron from dust, where bacteria promote dust dissolution by producing Fe-complexing molecules (siderophores) and
Trichodesmium
provides dust and optimal physical settings for dissolution and uptake. Our results demonstrate how intricate relationships between producers and consumers can influence productivity in the nutrient starved open ocean.
“…To assign significance in differential expression, Analysis of Sequence Counts (ASC) was used (Wu et al, 2010), with a fold change greater than or equal to 2 and a posterior probability (post- p ) > 0.95 as has been used in studies of similar design (Dyhrman et al, 2012; Thomas et al, 2012; Konotchick et al, 2013; Frischkorn et al, 2014; Alexander et al, 2015; Haley et al, 2017; Frischkorn et al, 2018). ASC is an empirical Bayes method that estimates the prior distribution by modeling biological variability using the data itself, rather than imposing a negative binomial distribution.…”
Harmful algal blooms (HABs) threaten ecosystems and human health worldwide. Controlling nitrogen inputs to coastal waters is a common HAB management strategy, as nutrient concentrations often suggest coastal blooms are nitrogen-limited. However, defining best nutrient management practices is a long-standing challenge: in part, because of difficulties in directly tracking the nutritional physiology of harmful species in mixed communities. Using metatranscriptome sequencing and incubation experiments, we addressed this challenge by assaying the
in situ
physiological ecology of the ecosystem destructive alga,
Aureococcus anophagefferens
. Here we show that gene markers of phosphorus deficiency were expressed
in situ
, and modulated by the enrichment of phosphorus, which was consistent with the observed growth rate responses. These data demonstrate the importance of phosphorus in controlling brown-tide dynamics, suggesting that phosphorus, in addition to nitrogen, should be evaluated in the management and mitigation of these blooms. Given that nutrient concentrations alone were suggestive of a nitrogen-limited ecosystem, this study underscores the value of directly assaying harmful algae
in situ
for the development of management strategies.
“…With more DIP available, these metabolic activities may no longer be required and transfer decreases. How tightly regulated these interactions are is not quite understood, but experiments on quorum sensing suggest that the activity of the cyanobacteria might be more than just the sum of abiotic factors but rather “a complex interplay of biotic and environmental factors” [73]. The overall capacity of the cyanobacteria to scavenge P might therefore not entirely depend on its own metabolic capacity but also on that of its associated microorganisms or microbiome.…”
Dinitrogen (N2) fixation is a major source of external nitrogen (N) to aquatic ecosystems and therefore exerts control over productivity. Studies have shown that N2 -fixers release freshly fixed N into the environment, but the causes for this N release are largely unclear. Here, we show that the availability of phosphate can directly affect the transfer of freshly fixed N to epibionts in filamentous, diazotrophic cyanobacteria. Stable-isotope incubations coupled to single-cell analyses showed that <1% and ~15% of freshly fixed N was transferred to epibionts of Aphanizomenon and Nodularia, respectively, at phosphate scarcity during a summer bloom in the Baltic Sea. When phosphate was added, the transfer of freshly fixed N to epibionts dropped to about half for Nodularia, whereas the release from Aphanizomenon increased slightly. At the same time, the growth rate of Nodularia roughly doubled, indicating that less freshly fixed N was released and was used for biomass production instead. Phosphate scarcity and the resulting release of freshly fixed N could explain the heavy colonization of Nodularia filaments by microorganisms during summer blooms. As such, the availability of phosphate may directly affect the partitioning of fixed N2 in colonies of diazotrophic cyanobacteria and may impact the interactions with their microbiome.
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