The aggregation of phytoplankton leads to the settling of particulate organic carbon in the form of marine snow, making it an important process in marine biogeochemical cycles. Diatoms >20 µm in size are considered to contribute appreciably to sinking particle fluxes due to aggregation and the production of transparent exopolymeric particles (TEP), the matrix for marine snow aggregates; however, it is not known whether nano-sized (2–20 µm) diatoms are able to aggregate and produce TEP. Here, we tested the aggregation and production of TEP by the nano-diatom Minutocellus polymorphus and investigated if interactions with bacteria influence aggregation by comparing axenic M. polymorphus cultures with co-cultures of the diatom with bacterial taxa known to colonize marine snow particles. We found that M. polymorphus form sinking aggregates and produce TEP comparably to other phytoplankton groups and that aggregation and TEP production were influenced depending on the species of bacteria added. Aggregation was enhanced in the presence of Marinobacter adhaerens HP15, but not in the presence of Pseudoalteromonas carrageenovora or Vibrio thalassae. Cell aggregation mediated by interactions with specific bacterial species are possible mechanisms behind the export of nano-sized diatoms, such as M. polymorphus, especially in oligotrophic open ocean regions where small phytoplankton dominate.
Heterotrophic Bacteria Enhance the Aggregation of the Marine Picocyanobacteria Prochlorococcus and Synechococcus
Marine picocyanobacteria are ubiquitous primary producers across the world’s oceans, and play a key role in the global carbon cycle. Recent evidence stemming from in situ investigations have shown that picocyanobacteria are able to sink out of the euphotic zone to depth, which has traditionally been associated with larger, mineral ballasted cells. The mechanisms behind the sinking of picocyanobacteria remain a point of contention, given that they are too small to sink on their own. To gain a mechanistic understanding of the potential role of picocyanobacteria in carbon export, we tested their ability to form “suspended” (5–60 μm) and “visible” (ca. > 0.1 mm) aggregates, as well as their production of transparent exopolymer particles (TEP)—which are a key component in the formation of marine aggregates. Additionally, we investigated if interactions with heterotrophic bacteria play a role in TEP production and aggregation in Prochlorococcus and Synechococcus by comparing xenic and axenic cultures. We observed TEP production and aggregation in batch cultures of axenic Synechococcus, but not in axenic Prochlorococcus. Heterotrophic bacteria enhanced TEP production as well as suspended and visible aggregate formation in Prochlorococcus, while in Synechococcus, aggregation was enhanced with no changes in TEP. Aggregation experiments using a natural plankton community dominated by picocyanobacteria resulted in aggregation only in the presence of the ballasting mineral kaolinite, and only when Synechococcus were in their highest seasonal abundance. Our results point to a different export potential between the two picocyanobacteria, which may be mediated by interactions with heterotrophic bacteria and presence of ballasting minerals. Further studies are needed to clarify the mechanistic role of bacteria in TEP production and aggregation of these picocyanobacteria.
more »
« less
- Award ID(s):
- 1658527
- NSF-PAR ID:
- 10228376
- Date Published:
- Journal Name:
- Frontiers in microbiology
- ISSN:
- 1664-302X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
Marine snow aggregates often dominate carbon export from the surface layer to the deep ocean. Therefore, understanding the formation and properties of aggregates is essential to the study of the biological pump. Previous studies have observed a relationship between phytoplankton growth phase and the production of transparent exopolymer particles (TEP), the sticky particles secreted by phytoplankton that act as the glue during aggregate formation. In this experimental study, we aim to determine the effect of phytoplankton growth phase on properties related to aggregate settling. Cultures of the diatom Thalassiosira weissflogii were grown to four different growth phases and incubated in rotating cylindrical tanks to form aggregates. Aggregate excess density and delayed settling time through a sharp density gradient were quantified for the aggregates that were formed, and relative TEP concentration was measured for cultures before aggregate formation. Compared to the first growth phase, later phytoplankton growth phases were found to have higher relative TEP concentration and aggregates with lower excess densities and longer delayed settling times. These findings may suggest that, although particle concentrations are higher at later stages of phytoplankton blooms, aggregates may be less dense and sink slower, thus affecting carbon export.more » « less
-
null (Ed.)Daily oscillations in photosynthetically active radiation strongly influence the timing of metabolic processes in picocyanobacteria, but it is less clear how the light-dark cycle affects the activities of their consumers. We investigated the relationship between marine picocyanobacteria and nanoplanktonic consumers throughout the diel cycle to determine whether heterotrophic and mixotrophic protists (algae with phagotrophic ability) display significant periodicity in grazing pressure. Carbon biomass of Prochlorococcus and Synechococcus was estimated continuously from abundances and cell size measurements made by flow cytometry. Picocyanobacterial dynamics were then compared to nanoplankton abundances and ingestion of fluorescently labeled bacteria measured every 4 h during a 4 d survey in the North Pacific Subtropical Gyre. Grazing of the labeled bacteria by heterotrophic nanoplankton was significantly greater at night than during the day. The grazing activity of mixotrophic nanoplankton showed no diel periodicity, suggesting that they may feed continuously, albeit at lower rates than heterotrophic nanoplankton, to alleviate nutrient limitation in this oligotrophic environment. Diel changes in Prochlorococcus biomass indicated that they could support substantial growth of nanoplankton if those grazers are the main source of picocyanobacterial mortality, and that grazers may contribute to temporally stable abundances of picocyanobacteria.more » « less
-
Martiny, Jennifer B. (Ed.)ABSTRACT The marine cyanobacterium Prochlorococcus numerically dominates the phytoplankton community of the nutrient-limited open ocean, establishing itself as the most abundant photosynthetic organism on Earth. This ecological success has been attributed to lower cell quotas for limiting nutrients, superior resource acquisition, and other advantages associated with cell size reduction and genome streamlining. In this study, we tested the prediction that Prochlorococcus outcompetes its rivals for scarce nutrients and that this advantage leads to its numerical success in nutrient-limited waters. Strains of Prochlorococcus and its sister genus Synechococcus grew well in both mono- and cocultures when nutrients were replete. However, in nitrogen-limited medium, Prochlorococcus outgrew Synechococcus but only when heterotrophic bacteria were also present. In the nitrogen-limited medium, the heterotroph Alteromonas macleodii outcompeted Synechococcus for nitrogen but only if stimulated by the exudate released by Prochlorococcus or if a proxy organic carbon source was provided. Genetic analysis of Alteromonas suggested that it outcompetes Synechococcus for nitrate and/or nitrite, during which cocultured Prochlorococcus grows on ammonia or other available nitrogen species. We propose that Prochlorococcus can stimulate antagonism between heterotrophic bacteria and potential phytoplankton competitors through a metabolic cross-feeding interaction, and this stimulation could contribute to the numerical success of Prochlorococcus in nutrient-limited regions of the ocean. IMPORTANCE In nutrient-poor habitats, competition for limited resources is thought to select for organisms with an enhanced ability to scavenge nutrients and utilize them efficiently. Such adaptations characterize the cyanobacterium Prochlorococcus , the most abundant photosynthetic organism in the nutrient-limited open ocean. In this study, the competitive superiority of Prochlorococcus over a rival cyanobacterium, Synechococcus , was captured in laboratory culture. Critically, this outcome was achieved only when key aspects of the open ocean were simulated: a limited supply of nitrogen and the presence of heterotrophic bacteria. The results indicate that Prochlorococcus promotes its numerical dominance over Synechococcus by energizing the heterotroph’s ability to outcompete Synechococcus for available nitrogen. This study demonstrates how interactions between trophic groups can influence interactions within trophic groups and how these interactions likely contribute to the success of the most abundant photosynthetic microorganism.more » « less
-
Johnson, Karyn N. (Ed.)ABSTRACT Coral reefs are possible sinks for microbes; however, the removal mechanisms at play are not well understood. Here, we characterize pelagic microbial groups at the CARMABI reef (Curaçao) and examine microbial consumption by three coral species: Madracis mirabilis , Porites astreoides , and Stephanocoenia intersepta . Flow cytometry analyses of water samples collected from a depth of 10 m identified 6 microbial groups: Prochlorococcus , three groups of Synechococcus , photosynthetic eukaryotes, and heterotrophic bacteria. Minimum growth rates (μ) for Prochlorococcus , all Synechococcus groups, and photosynthetic eukaryotes were 0.55, 0.29, and 0.45 μ day −1 , respectively, and suggest relatively high rates of productivity despite low nutrient conditions on the reef. During a series of 5-h incubations with reef corals performed just after sunset or prior to sunrise, reductions in the abundance of photosynthetic picoeukaryotes, Prochlorococcus and Synechococcus cells, were observed. Of the three Synechococcus groups, one decreased significantly during incubations with each coral and the other two only with M. mirabilis. Removal of carbon from the water column is based on coral consumption rates of phytoplankton and averaged between 138 ng h −1 and 387 ng h −1 , depending on the coral species. A lack of coral-dependent reduction in heterotrophic bacteria, differences in Synechococcus reductions, and diurnal variation in reductions of Synechococcus and Prochlorococcus , coinciding with peak cell division, point to selective feeding by corals. Our study indicates that bentho-pelagic coupling via selective grazing of microbial groups influences carbon flow and supports heterogeneity of microbial communities overlying coral reefs. IMPORTANCE We identify interactions between coral grazing behavior and the growth rates and cell abundances of pelagic microbial groups found surrounding a Caribbean reef. During incubation experiments with three reef corals, reductions in microbial cell abundance differed according to coral species and suggest specific coral or microbial mechanisms are at play. Peaks in removal rates of Prochlorococcus and Synechococcus cyanobacteria appear highest during postsunset incubations and coincide with microbial cell division. Grazing rates and effort vary across coral species and picoplankton groups, possibly influencing overall microbial composition and abundance over coral reefs. For reef corals, use of such a numerically abundant source of nutrition may be advantageous, especially under environmentally stressful conditions when symbioses with dinoflagellate algae break down.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fmicb.2019.01864
