skip to main content


Title: A tripartite model system for Southern Ocean diatom-bacterial interactions reveals the coexistence of competing symbiotic strategies
Abstract

Southern Ocean (SO) diatoms play an important role in global carbon flux, and their influence on carbon export is directly linked to interactions with epiphytic bacteria. Bacterial symbionts that increase diatom growth promote atmospheric carbon uptake, while bacterial degraders divert diatom biomass into the microbial loop where it can then be released as carbon dioxide through respiration. To further explore SO diatom-bacterial associations, a natural model system is needed that is representative of these diverse and important interactions. Here, we use concurrent cultivation to isolate a species of the ecologically-important SO diatom, Pseudo-nitzschia subcurvata, and its co-occurring bacteria. Although vitamin-depleted, axenic Pseudo-nitzschia grew poorly in culture, addition of a co-isolated Roseobacter promoted diatom growth, while addition of a co-isolated Flavobacterium negatively impacted diatom growth. Microscopy revealed both bacterial isolates are physically associated with diatom cells and genome sequencing identified important predicted functions including vitamin synthesis, motility, cell attachment mechanisms, and diverse antimicrobial weapons that could be used for interbacterial competition. These findings revealed the natural coexistence of competing symbiotic strategies of diatom-associated bacteria in the SO, and the utility of this tripartite system, composed of a diatom and two bacterial strains, as a co-culture model to probe ecological-relevant interactions between diatoms and the bacteria that compete for access to the phycosphere.

 
more » « less
Award ID(s):
1745036
NSF-PAR ID:
10372795
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
ISME Communications
Volume:
2
Issue:
1
ISSN:
2730-6151
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. The growth of diatoms in the Southern Ocean, especially the region surrounding the West Antarctic Peninsula, is frequently constrained by low dissolved iron and other trace metal concentrations. This challenge may be overcome by mutualisms between diatoms and co-occurring associated bacteria, in which diatoms produce organic carbon as a substrate for bacterial growth, and bacteria produce siderophores, metal-binding ligands that can supply diatoms with metals upon uptake as well as other useful secondary compounds for diatom growth like vitamins. To examine the relationships between diatoms and bacteria in the plankton (diatom) size class (> 3 µm), we sampled both bacterial and diatom community composition with accompanying environmental metadata across a naturally occurring concentration gradient of macronutrients, trace metals and siderophores at 21 stations near the West Antarctic Peninsula (WAP). Offshore Drake Passage stations had low dissolved iron (0.33 ± 0.15 nM), while the stations closer to the continental margin had higher dissolved iron (5.05 ± 1.83 nM). A similar geographic pattern was observed for macronutrients and most other trace metals measured, but there was not a clear inshore-offshore gradient in siderophore concentrations. The diatom and bacteria assemblages, determined using 18S and 16S rDNA sequencing respectively, were similar by location sampled, and variance in both assemblages was driven in part by concentrations of soluble reactive phosphorous, dissolved manganese, and dissolved copper, which were all higher near the continent. Some of the most common diatom sequence types observed were Thalassiosira and Fragilariopsis , and bacteria in the plankton size fraction were most commonly Bacteroidetes and Gammaproteobacteria. Network analysis showed positive associations between diatoms and bacteria, indicating possible in situ mutualisms through strategies such as siderophore and vitamin biosynthesis and exchange. This work furthers the understanding of how naturally occurring gradients of metals and nutrients influence diatom-bacteria interactions. Our data suggest that distinct groups of diatoms and associated bacteria are interacting under different trace metal regimes in the WAP, and that diatoms with different bacterial partners may have different modes of biologically supplied trace metals. 
    more » « less
  2. Gralnick, Jeffrey A. (Ed.)
    ABSTRACT Microalgal cultures are often maintained in xenic conditions, i.e., with associated bacteria, and many studies indicate that these communities both are complex and have significant impacts on the physiology of the target photoautotroph. Here, we investigated the structure and stability of microbiomes associated with a diverse sampling of diatoms during long-term maintenance in serial batch culture. We found that, counter to our initial expectation, evenness diversity increased with time since cultivation, driven by a decrease in dominance by the most abundant taxa in each culture. We also found that the site from which and time at which a culture was initially collected had a stronger impact on microbiome structure than the diatom species; however, some bacterial taxa were commonly present in most cultures despite having widely geographically separated collection sites. Our results support the conclusion that stochastic initial conditions (i.e., the local microbial community at the collection site) are important for the long-term structure of these microbiomes, but deterministic forces such as negative frequency dependence and natural selection exerted by the diatom are also at work. IMPORTANCE Natural microbial communities are extremely complex, with many more species coexisting in the same place than there are different resources to support them. Understanding the forces that allow this high level of diversity has been a central focus of ecological and evolutionary theory for many decades. Here, we used stock cultures of diatoms, which were maintained for years in continuous growth alongside populations of bacteria, as proxies for natural communities. We show that the bacterial communities remained relatively stable for years, and there is evidence that ecological forces worked to stabilize coexistence instead of favoring competition and exclusion. We also show evidence that, despite some important regional differences in bacterial communities, there was a globally present core microbiome potentially selected for in these diatom cultures. Understanding interactions between bacteria and diatoms is important both for basic ecological science and for practical science, such as industrial biofuel production. 
    more » « less
  3. null (Ed.)
    The Southern Ocean (SO) harbors some of the most intense phytoplankton blooms on Earth. Changes in temperature and iron availability are expected to alter the intensity of SO phytoplankton blooms, but little is known about how these changes will influence community composition and downstream biogeochemical processes. We performed light-saturated experimental manipulations on surface ocean microbial communities from McMurdo Sound in the Ross Sea to examine the effects of increased iron availability (+2 nM) and warming (+3 and +6 °C) on nutrient uptake, as well as the growth and transcriptional responses of two dominant diatoms, Fragilariopsis and Pseudo-nitzschia . We found that community nutrient uptake and primary productivity were elevated under both warming conditions without iron addition (relative to ambient −0.5 °C). This effect was greater than additive under concurrent iron addition and warming. Pseudo-nitzschia became more abundant under warming without added iron (especially at 6 °C), while Fragilariopsis only became more abundant under warming in the iron-added treatments. We attribute the apparent advantage Pseudo-nitzschia shows under warming to up-regulation of iron-conserving photosynthetic processes, utilization of iron-economic nitrogen assimilation mechanisms, and increased iron uptake and storage. These data identify important molecular and physiological differences between dominant diatom groups and add to the growing body of evidence for Pseudo-nitzschia ’s increasingly important role in warming SO ecosystems. This study also suggests that temperature-driven shifts in SO phytoplankton assemblages may increase utilization of the vast pool of excess nutrients in iron-limited SO surface waters and thereby influence global nutrient distribution and carbon cycling. 
    more » « less
  4. Abstract

    The importance of zinc (Zn) as a nutrient and its ability to be substituted for by cobalt (Co) have been characterized in model marine diatoms. However, the extent to which this substitution capability is distributed among diatom taxa is unknown. Zn/Co metabolic substitution was assayed in four diatom species as measured by the effect of free ion concentrations of Zn2+and Co2+on specific growth rate. Analysis of growth responses found substitution of these metals can occur within the northwest Atlantic isolateThalassiosira pseudonanaCCMP1335, the northeast Atlantic isolatePhaeodactylum tricornutumCCMP632, and within the northeast Pacific isolatesPseudo‐nitzschia delicatissimaUNC1205 andThalassiosirasp. UNC1203. Metabolic substitution of Co in place of Zn in the Atlantic diatoms supports their growth in media lacking added Zn, but at the cost of reduced growth rates. In contrast, highly efficient Zn/Co substitution that supported growth even in media lacking added Zn was observed in the northeast Pacific diatoms. We also present new data from the northeast Pacific Line P transect that revealed dissolved Co and Zn ratios (dCo : dZn) as high as 3.52 : 1 at surface (0–100 m) depths. We posit that the enhanced ability of the NE Pacific diatoms to grow using Co is an adaptation to these high surface dCo : dZn ratios. Particulate metal data and single‐cell metal quotas also suggest a high Zn demand in diatoms that may be partially compensated for by Co.

     
    more » « less
  5. Abstract

    Short timescale observations are valuable for understanding microbial ecological processes. We assessed dynamics in relative abundance and potential activities by sequencing the small sub-unit ribosomal RNA gene (rRNA gene) and rRNA molecules (rRNA) of Bacteria, Archaea, and Eukaryota once to twice daily between March 2014 and May 2014 from the surface ocean off Catalina Island, California. Typically Ostreococcus, Braarudosphaera, Teleaulax, and Synechococcus dominated phytoplankton sequences (including chloroplasts) while SAR11, Sulfitobacter, and Fluviicola dominated non-phytoplankton Bacteria and Archaea. We observed short-lived increases of diatoms, mostly Pseudo-nitzschia and Chaetoceros, with quickly responding Bacteria and Archaea including Flavobacteriaceae (Polaribacter & Formosa), Roseovarius, and Euryarchaeota (MGII), notably the exact amplicon sequence variants we observed responding similarly to another diatom bloom nearby, 3 years prior. We observed correlations representing known interactions among abundant phytoplankton rRNA sequences, demonstrating the biogeochemical and ecological relevance of such interactions: (1) The kleptochloroplastidic ciliate Mesodinium 18S rRNA gene sequences and a single Teleaulax taxon (via 16S rRNA gene sequences) were correlated (Spearman r = 0.83) yet uncorrelated to a Teleaulax 18S rRNA gene OTU, or any other taxon (consistent with a kleptochloroplastidic or karyokleptic relationship) and (2) the photosynthetic prymnesiophyte Braarudosphaera bigelowii and two strains of diazotrophic cyanobacterium UCYN-A were correlated and each taxon was also correlated to other taxa, including B. bigelowii to a verrucomicrobium and a dictyochophyte phytoplankter (all r > 0.8). We also report strong correlations (r > 0.7) between various ciliates, bacteria, and phytoplankton, suggesting interactions via currently unknown mechanisms. These data reiterate the utility of high-frequency time series to show rapid microbial reactions to stimuli, and provide new information about in situ dynamics of previously recognized and hypothesized interactions.

     
    more » « less