Species interaction networks are shaped by abiotic and biotic factors. Here, as part of the Tara Oceans project, we studied the photic zone interactome using environmental factors and organismal abundance profiles and found that environmental factors are incomplete predictors of community structure. We found associations across plankton functional types and phylogenetic groups to be nonrandomly distributed on the network and driven by both local and global patterns. We identified interactions among grazers, primary producers, viruses, and (mainly parasitic) symbionts and validated network-generated hypotheses using microscopy to confirm symbiotic relationships. We have thus provided a resource to support further research on ocean food webs and integrating biological components into ocean models.
Acylhomoserine lactone (AHLs)-mediated quorum-sensing (QS) processes seem to be common in the marine environment and among marine pathogenic bacteria, but no data are available on the prevalence of bacteria capable of interfering with QS in the sea, a process that has been generally termed 'quorum quenching' (QQ). One hundred and sixty-six strains isolated from different marine dense microbial communities were screened for their ability to interfere with AHL activity. Twenty-four strains (14.4%) were able to eliminate or significantly reduce N-hexanoyl-l-homoserine lactone activity as detected by the biosensor strain Chromobacterium violaceum CV026, a much higher percentage than that reported for soil isolates, which reinforces the ecological role of QS and QQ in the marine environment. Among these, 15 strains were also able to inhibit N-decanoyl-l-homoserine lactone activity and all of them were confirmed to enzymatically inactivate the AHL signals by HPLC-MS. Active isolates belonged to nine different genera of prevalently or exclusively marine origin, including members of the Alpha- and Gammaproteobacteria (8), Actinobacteria (2), Firmicutes (4) and Bacteroidetes (1). Whether the high frequency and diversity of cultivable bacteria with QQ activity found in near-shore marine isolates reflects their prevalence among pelagic marine bacterial communities deserves further investigation in order to understand the ecological importance of AHL-mediated QS and QQ processes in the marine environment.
The unicellular cyanobacterium UCYN-A, one of the major contributors to nitrogen fixation in the open ocean, lives in symbiosis with single-celled phytoplankton. UCYN-A includes several closely related lineages whose partner fidelity, genome-wide expression and time of evolutionary divergence remain to be resolved. Here we detect and distinguish UCYN-A1 and UCYN-A2 lineages in symbiosis with two distinct prymnesiophyte partners in the South Atlantic Ocean. Both symbiotic systems are lineage specific and differ in the number of UCYN-A cells involved. Our analyses infer a streamlined genome expression towards nitrogen fixation in both UCYN-A lineages. Comparative genomics reveal a strong purifying selection in UCYN-A1 and UCYN-A2 with a diversification process ∼91 Myr ago, in the late Cretaceous, after the low-nutrient regime period occurred during the Jurassic. These findings suggest that UCYN-A diversified in a co-evolutionary process, wherein their prymnesiophyte partners acted as a barrier driving an allopatric speciation of extant UCYN-A lineages.
A marine symbiosis has been recently discovered between prymnesiophyte species and the unicellular diazotrophic cyanobacterium UCYN-A. At least two different UCYN-A phylotypes exist, the clade UCYN-A1 in symbiosis with an uncultured small prymnesiophyte and the clade UCYN-A2 in symbiosis with the larger Braarudosphaera bigelowii. We targeted the prymnesiophyte-UCYN-A1 symbiosis by double CARD-FISH (catalyzed reporter deposition-fluorescence in situ hybridization) and analyzed its abundance in surface samples from the MALASPINA circumnavigation expedition. Our use of a specific probe for the prymnesiophyte partner allowed us to verify that this algal species virtually always carried the UCYN-A symbiont, indicating that the association was also obligate for the host. The prymnesiophyte-UCYN-A1 symbiosis was detected in all ocean basins, displaying a patchy distribution with abundances (up to 500 cells ml − 1 ) that could vary orders of magnitude. Additional vertical profiles taken at the NE Atlantic showed that this symbiosis occupied the upper water column and disappeared towards the Deep Chlorophyll Maximum, where the biomass of the prymnesiophyte assemblage peaked. Moreover, sequences of both prymnesiophyte partners were searched within a large 18S rDNA metabarcoding data set from the Tara-Oceans expedition around the world. This sequence-based analysis supported the patchy distribution of the UCYN-A1 host observed by CARD-FISH and highlighted an unexpected homogeneous distribution (at low relative abundance) of B. bigelowii in the open ocean. Our results demonstrate that partners are always in symbiosis in nature and show contrasted ecological patterns of the two related lineages.
We examine the large-scale distribution patterns of the nano- and microphytoplankton collected from 145 oceanic stations, at 3 m depth, the 20% light level and the depth of the subsurface chlorophyll maximum, during the Malaspina-2010 Expedition (December 2010-July 2011), which covered 15 biogeographical provinces across the Atlantic, Indian and Pacific oceans, between 35°N and 40°S. In general, the water column was stratified, the surface layers were nutrient-poor and the nano- and microplankton (hereafter phytoplankton, for simplicity, although it included also heterotrophic protists) community was dominated by dinoflagellates, other flagellates and coccolithophores, while the contribution of diatoms was only important in zones with shallow nutriclines such as the equatorial upwelling regions. We applied a principal component analysis to the correlation matrix among the abundances (after logarithmic transform) of the 76 most frequent taxa to synthesize the information contained in the phytoplankton data set. The main trends of variability identified consisted of: 1) A contrast between the community composition of the upper and the lower parts of the euphotic zone, expressed respectively by positive or negative scores of the first principal component, which was positively correlated with taxa such as the dinoflagellates Oxytoxum minutum and Scrippsiella spp., and the coccolithophores Discosphaera tubifera and Syracosphaera pulchra (HOL and HET), and negatively correlated with taxa like Ophiaster hydroideus (coccolithophore) and several diatoms, 2) a general abundance gradient between phytoplankton-rich regions with high abundances of dinoflagellate, coccolithophore and ciliate taxa, and phytoplankton-poor regions (second principal component), 3) differences in dominant phytoplankton and ciliate taxa among the Atlantic, the Indian and the Pacific oceans (third principal component) and 4) the occurrence of a diatom-dominated assemblage (the fourth principal component assemblage), including several pennate taxa, Planktoniella sol, Hemiaulus hauckii and Pseudo-nitzschia spp., in the divergence regions. Our findings indicate that consistent assemblages of co-occurring phytoplankton taxa can be identified and that their distribution is best explained by a combination in different degrees of both environmental and historical influences.
The fine vertical distribution of phytoplankton groups within the deep chlorophyll maximum (DCM) was studied in the NE Atlantic during summer stratification. A simple but unconventional sampling strategy allowed examining the vertical structure with ca. 2 m resolution. The distribution of Prochlorococcus, Synechococcus, chlorophytes, pelagophytes, small prymnesiophytes, coccolithophores, diatoms, and dinoflagellates was investigated with a combination of pigment-markers, flow cytometry and optical and FISH microscopy. All groups presented minimum abundances at the surface and a maximum in the DCM layer. The cell distribution was not vertically symmetrical around the DCM peak and cells tended to accumulate in the upper part of the DCM layer. The more symmetrical distribution of chlorophyll than cells around the DCM peak was due to the increase of pigment per cell with depth. We found a vertical alignment of phytoplankton groups within the DCM layer indicating preferences for different ecological niches in a layer with strong gradients of light and nutrients. Prochlorococcus occupied the shallowest and diatoms the deepest layers. Dinoflagellates, Synechococcus and small prymnesiophytes preferred shallow DCM layers, and coccolithophores, chlorophytes and pelagophytes showed a preference for deep layers. Cell size within groups changed with depth in a pattern related to their mean size: the cell volume of the smallest group increased the most with depth while the cell volume of the largest group decreased the most. The vertical alignment of phytoplankton groups confirms that the DCM is not a homogeneous entity and indicates groups' preferences for different ecological niches within this layer.The deep chlorophyll maximum (DCM) is a subsurface layer enriched in chlorophyll (Chl) typical of stratified marine and freshwater bodies. It might be the result of diverse processes and may present different characteristics (Cullen 1982(Cullen , 2015. In temperate areas, the DCM disappears in winter when mixing takes place and reappears after the spring bloom, when stratification is established. The dynamics of this kind of DCM have been described in the literature (Estrada et al. 1993;Mignot et al. 2014). Briefly, winter surface waters replete with nutrients start stratifying after the air-water heat balance becomes negative (Sverdrup 1953;Taylor and Ferrari 2011) producing the spring bloom in temperate areas (although this classical approach has been challenged by Behrenfeld 2010). At this moment, the abundant phytoplankton accumulates very close to the surface, limiting the irradiance immediately below and inducing the synthesis of pigments by the deeper phytoplankton and the formation of a shallow DCM that might not correspond to a biomass maximum. However, this is a very dynamic situation because phytoplankton quickly (days-weeks) consume the nutrients from the well illuminated layers becoming less abundant at surface and concentrating at depth. This process originates a deeper DCM, coinciding with the nutricline ...
In the last decade, the known biogeography of nitrogen fixation in the ocean has been expanded to colder and nitrogen‐rich coastal environments. The symbiotic nitrogen‐fixing cyanobacteria group A (UCYN‐A) has been revealed as one of the most abundant and widespread nitrogen‐fixers, and includes several sublineages that live associated with genetically distinct but closely related prymnesiophyte hosts. The UCYN‐A1 sublineage is associated with an open ocean picoplanktonic prymnesiophyte, whereas UCYN‐A2 is associated with the coastal nanoplanktonic coccolithophore Braarudosphaera bigelowii , suggesting that different sublineages may be adapted to different environments. Here, we study the diversity of nifH genes present at the Santa Cruz Municipal Wharf in the Monterey Bay (MB), California, and report for the first time the presence of multiple UCYN‐A sublineages, unexpectedly dominated by the UCYN‐A2 sublineage. Sequence and quantitative PCR data over an 8‐year time‐series (2011–2018) showed a shift toward increasing UCYN‐A2 abundances after 2013, and a marked seasonality for this sublineage which was present during summer‐fall months, coinciding with the upwelling‐relaxation period in the MB. Increased abundances corresponded to positive temperature anomalies in MB, and we discuss the possibility of a benthic life stage of the associated coccolithophore host to explain the seasonal pattern. The dominance of UCYN‐A2 in coastal waters of the MB underscores the need to further explore the habitat preference of the different sublineages in order to provide additional support for the hypothesis that UCYN‐A1 and UCYN‐A2 sublineages are different ecotypes.
The symbiotic N2-fixing cyanobacterium UCYN-A, which is closely related to Braarudosphaera bigelowii, and its eukaryotic algal host have been shown to be globally distributed and important in open-ocean N2 fixation. These unique cyanobacteria have reduced metabolic capabilities, even lacking genes for oxygenic photosynthesis and carbon fixation. Cyanobacteria generally use energy from photosynthesis for nitrogen fixation but require mechanisms for avoiding inactivation of the oxygen-sensitive nitrogenase enzyme by ambient oxygen (O2) or the O2 evolved through photosynthesis. This study showed that symbiosis between the N2-fixing cyanobacterium UCYN-A and its eukaryotic algal host has led to adaptation of its daily gene expression pattern in order to enable daytime aerobic N2 fixation, which is likely more energetically efficient than fixing N2 at night, as found in other unicellular marine cyanobacteria.
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