Global Phylogeography of Marine
            <i>Synechococcus</i>
            in Coastal Areas Reveals Strong Community Shifts

Doré, Hugo; Leconte, Jade; Guyet, Ulysse; Breton, Solène; Farrant, Gregory K.; Demory, David; Ratin, Morgane; Hoebeke, Mark; Corre, Erwan; Pitt, Frances Diana; Ostrowski, Martin; Scanlan, David J.; Partensky, Frédéric; Six, Christophe; Garczarek, Laurence

doi:10.1128/msystems.00656-22

Cited by 15 publications

(19 citation statements)

References 84 publications

(165 reference statements)

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“…The presence of psip1 in marine picocyanobacteria is restricted to marine Synechococcus (clade III) and some HLI Prochlorococcus (e.g., MED4 and EQPAC1). Members of Synechococcus clade III are well described as preferentially occupying P-depleted oligotrophic waters ( 18 , 59 ) and hence carriage of psip1 specifically in these strains is consistent with this being a niche-specific gene. In Prochlorococcus sp.…”

Section: Resultssupporting

confidence: 56%

A distinct, high-affinity, alkaline phosphatase facilitates occupation of P-depleted environments by marine picocyanobacteria

Torcello-Requena,

Murphy,

Lidbury

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus , the two most abundant phototrophs on Earth, thrive in oligotrophic oceanic regions. While it is well known that specific lineages are exquisitely adapted to prevailing in situ light and temperature regimes, much less is known of the molecular machinery required to facilitate occupancy of these low-nutrient environments. Here, we describe a hitherto unknown alkaline phosphatase, Psip1, that has a substantially higher affinity for phosphomonoesters than other well-known phosphatases like PhoA, PhoX, or PhoD and is restricted to clade III Synechococcus and a subset of high light I-adapted Prochlorococcus strains, suggesting niche specificity. We demonstrate that Psip1 has undergone convergent evolution with PhoX, requiring both iron and calcium for activity and likely possessing identical key residues around the active site, despite generally very low sequence homology. Interrogation of metagenomes and transcriptomes from TARA oceans and an Atlantic Meridional transect shows that psip1 is abundant and highly expressed in picocyanobacterial populations from the Mediterranean Sea and north Atlantic gyre, regions well recognized to be phosphorus (P)-deplete. Together, this identifies psip1 as an important oligotrophy-specific gene for P recycling in these organisms. Furthermore, psip1 is not restricted to picocyanobacteria and is abundant and highly transcribed in some α-proteobacteria and eukaryotic algae, suggesting that such a high-affinity phosphatase is important across the microbial taxonomic world to occupy low-P environments.

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Section: Resultssupporting

confidence: 56%

A distinct, high-affinity, alkaline phosphatase facilitates occupation of P-depleted environments by marine picocyanobacteria

Torcello-Requena,

Murphy,

Lidbury

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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“…The Synechococcus community at MVCO is dominated year-round by a single clade (Hunter-Cevera et al 2016b), which we might expect to grow in conditions across the shelf. Coastal microbial community composition can vary across short distances, however, with both temperature and distance from shore (Wang et al 2019;Doré et al 2022). It may be that Synechococcus strains with different reproductive strategies are abundant in the offshore region despite dividing less rapidly.…”

Section: Drivers and Controlsmentioning

confidence: 99%

Temperature regulates Synechococcus population dynamics seasonally and across the continental shelf

Stevens

Crockford

Peacock

et al. 2023

Limnol Oceanogr Letters

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Hourly, year‐round flow cytometry has made it possible to relate seasonal environmental variability to the population dynamics of the smallest, most abundant phytoplankton on the Northeast US Shelf. To evaluate whether the insights from these data extend to Synechococcus farther from shore, we analyze flow cytometry measurements made continuously from the underway systems on 21 cruises traveling between the Martha's Vineyard Coastal Observatory (MVCO) and the continental shelf break. We describe how seasonal patterns in Synechococcus, which have been documented in detail at MVCO, occur across the region with subtle variation. We find that the underlying relationship between temperature and division rate is consistent across the shelf and can explain much of the observed spatial variability in concentration. Connecting individual cell properties to annual and regional patterns in environmental conditions, these results demonstrate the value of autonomous monitoring and create an improved picture of picophytoplankton dynamics within an economically important ecosystem.

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“…The picoeukaryotes are a diverse group (Díez et al., 2001; Moon‐van Der Staay et al., 2001; Zeidner et al., 2003), and it is very likely that our flow cytometry measurements are summarizing multiple taxa. While we might expect a taxon to invade the offshore waters if it were capable of dividing more rapidly under the offshore conditions, we know that coastal microbial community composition can vary across short distances and may not reflect an ecologically stable state (Doré et al., 2022; Wang et al., 2019). We will therefore discuss two physiological explanations for the observed patterns, while recognizing that taxonomic differences may also be at play.…”

Section: Discussionmentioning

confidence: 99%

Distinct responses to warming within picoplankton communities across an environmental gradient

Stevens,

Peacock,

Crockford

et al. 2024

Global Change Biology

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Picophytoplankton are a ubiquitous component of marine plankton communities and are expected to be favored by global increases in seawater temperature and stratification associated with climate change. Eukaryotic and prokaryotic picophytoplankton have distinct ecology, and global models predict that the two groups will respond differently to future climate scenarios. At a nearshore observatory on the Northeast US Shelf, however, decades of year‐round monitoring have shown these two groups to be highly synchronized in their responses to environmental variability. To reconcile the differences between regional and global predictions for picophytoplankton dynamics, we here investigate the picophytoplankton community across the continental shelf gradient from the nearshore observatory to the continental slope. We analyze flow cytometry data from 22 research cruises, comparing the response of picoeukaryote and Synechococcus communities to environmental variability across time and space. We find that the mechanisms controlling picophytoplankton abundance differ across taxa, season, and distance from shore. Like the prokaryote, Synechococcus, picoeukaryote division rates are limited nearshore by low temperatures in winter and spring, and higher temperatures offshore lead to an earlier spring bloom. Unlike Synechococcus, picoeukaryote concentration in summer decreases dramatically in offshore surface waters and exhibits deeper subsurface maxima. The offshore picoeukaryote community appears to be nutrient limited in the summer and subject to much greater loss rates than Synechococcus. This work both produces and demonstrates the necessity of taxon‐ and site‐specific knowledge for accurately predicting the responses of picophytoplankton to ongoing environmental change.

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Global Phylogeography of Marine Synechococcus in Coastal Areas Reveals Strong Community Shifts

Cited by 15 publications

References 84 publications

A distinct, high-affinity, alkaline phosphatase facilitates occupation of P-depleted environments by marine picocyanobacteria

A distinct, high-affinity, alkaline phosphatase facilitates occupation of P-depleted environments by marine picocyanobacteria

Temperature regulates Synechococcus population dynamics seasonally and across the continental shelf

Distinct responses to warming within picoplankton communities across an environmental gradient

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