Latitudinal constraints on the abundance and activity of the cyanobacterium UCYN‐A and other marine diazotrophs in the North Pacific

Gradoville, Mary R.; Farnelid, Hanna; White, Angelicque E.; Turk‐Kubo, Kendra A.; Stewart, Breanne; Ribalet, François; Ferrón, Sara; Pinedo‐González, Paulina; Armbrust, E. Virginia; Karl, David M.; John, Seth G.; Zehr, Jonathan P.

doi:10.1002/lno.11423

Cited by 45 publications

(86 citation statements)

References 115 publications

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“…In a non-metric multidimensional scaling (NMDS) analysis where each metabolite was treated with equal weight, there was a distinct shift in metabolite patterns in the samples on either side of approximately 30 • N ( Figure S2, ANOSIM stat = 0.316, p = 0.005). This corresponds well with the southern boundary of the North Pacific Transition Zone, a well described oceanographic feature which extends from Japan to North America and arises from large-scale ocean circulation (26,27). The northern and southern edges of this transition zone comprise of rapid changes in thermohaline structure and biological species composition (28,26,29).…”

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confidence: 64%

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Marine community metabolomes carry fingerprints of phytoplankton community composition

Durham

Boysen

Carlson

et al. 2020

Preprint

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Phytoplankton transform inorganic carbon into thousands of biomolecules that represent an important pool of fixed carbon, nitrogen, and sulfur in the surface ocean. Metabolite production differs between phytoplankton, and the flux of these molecules through the microbial food web depends on compound-specific bioavailability to members of a wider microbial community. Yet relatively little is known about the diversity or concentration of metabolites within marine plankton. Here we compare 313 polar metabolites in 21 cultured phytoplankton species and in natural planktonic communities across environmental gradients to show that bulk community metabolomes reflect chemical composition of the phytoplankton community. We also show that groups of compounds have similar patterns across space and taxonomy suggesting that the concentrations of these compounds in the environment are controlled by similar sources and sinks. We quantify several compounds in the surface ocean that represent substantial understudied pools of labile carbon. For example, the N-containing metabolite homarine was up to 3% of particulate carbon and is produced in high concentrations by cultured Synechococcus, and S-containing gonyol accumulated up to 2.5 nM in surface particles and likely originates from dinoflagellates. Our results show that phytoplankton composition directly shapes the carbon composition of the surface ocean. Our findings suggest that in order to access these pools of bioavailable carbon, the wider microbial community must be adapted to phytoplankton community composition.IMPORTANCEMicroscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet, the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Here we explore the abundance and diversity of small biomolecules in planktonic communities across ecological gradients in the North Pacific and within 21 cultured phytoplankton species. Our work demonstrates that phytoplankton diversity is an important determinant of the chemical composition of the highly bioavailable pool of organic carbon in the ocean, and we highlight understudied yet abundant compounds in both the environment and cultured organisms. These findings add to understanding of how the chemical makeup of phytoplankton shapes marine microbial communities where the ability to sense and use biomolecules depends on the chemical structure.

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confidence: 64%

“…-37.3 11.4-17.1 34.1-34.7 0.06-5.87 0.07-0.51 0.16-0.37 Summary of physical and chemical parameters on April 2016 cruise. Reprinted with permission from(27).…”

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Marine community metabolomes carry fingerprints of phytoplankton community composition

Durham

Boysen

Carlson

et al. 2020

Preprint

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“…While the domain of marine BNF has been broadened with ongoing studies and active BNF in the Arctic region (Harding et al, 2018; Shiozaki et al, 2018; Sipler et al, 2017), diazotrophs and BNF were found to be rare or absent in the NPTZ where constitutes approximately 12% of the surface area of the North Pacific Ocean (Church et al, 2008; Gradoville et al, 2020; Shiozaki et al, 2017). The most recent survey of diazotrophs in the NPTZ was conducted along latitudinal transects in the central Pacific along 160°W during spring (Gradoville et al, 2020), in which the diazotroph abundance decreased suddenly at the southern edge of the NPTZ (~32°N) and became rare or undetected in the NPTZ (~32–40°N). A similar study conducted along 170°W also found undetectable diazotroph abundance with qPCR and relatively low BNF in the NPTZ between 35 and 40°N (Shiozaki et al, 2017).…”

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confidence: 99%

Physical Forcing Controls the Basin‐Scale Occurrence of Nitrogen‐Fixing Organisms in the North Pacific Ocean

Cheung

Nitanai

Tsurumoto

et al. 2020

Global Biogeochemical Cycles

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Biological nitrogen fixation is increasingly recognized as an important source of new nitrogen in a warming ocean. However, the basin-scale spatiotemporal distribution of nitrogen-fixing organisms (diazotrophs) in the ocean and its controlling environmental factors remain unclear. Here we examined the basin-scale seasonal distribution patterns of major diazotrophs (filamentous cyanobacterial Trichodesmium, unicellular cyanobacterial UCYN-A1, and proteobacterial Gamma-A) in surface waters of the North Pacific from 2014 to 2016 with unprecedented coverage and resolution. In general, UCYN-A1, Trichodesmium, and Gamma-A were abundant during spring-autumn, summer-autumn, and spring respectively. Regarding latitudinal patterns of abundance, UCYN-A1 showed dome shape; Trichodesmium was gradually decreasing from low-to high-latitude regions; and Gamma-A did not show a clear pattern, which were coincident with the distinct correlations between the diazotrophs and temperature. All three diazotrophs were abundant (reached 10 6-10 7 nifH gene copy number L −1) in the North Pacific transition zone and subtropical gyre, where the cyanobacterial diazotrophs were more abundant in both the western and eastern North Pacific than in the central North Pacific. The diazotroph abundance in the western North Pacific was positively correlated with eddy kinetic energy and sea surface height anomaly, which implies an enhancement of diazotrophs in mesoscale eddies associated with the western boundary current Kuroshio and its extension. The cyanobacterial diazotrophs were positively correlated with wind stress curl, a measurable parameter of wind-driven upwelling, in the eastern North Pacific. Our study refines the biogeography of three major diazotrophs and highlights the importance of physical forcing in mediating their dynamics.

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“…For most sample sets, complementary sequence data were available to determine whether UCYN-A2 or UCYN-A3 was present. This figure was modified from Farnelid et al 2016, and updated to include data from Hagino et al 2013, Shiozaki et al 2017, 2018, Stenegren et al 2018, Berthelot et al 2017, Henke et al 2018, Harding et al 2018, Gradoville et al 2020, and this work.…”

Section: Fig 1 Map Of Distribution Of Ucyn-a In the Pacific And Arcticmentioning

confidence: 99%

Unexpected presence of the nitrogen‐fixing symbiotic cyanobacterium UCYN‐A in Monterey Bay, California

Cabello

Turk‐Kubo

Hayashi

et al. 2020

Journal of Phycology

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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.

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Latitudinal constraints on the abundance and activity of the cyanobacterium UCYN‐A and other marine diazotrophs in the North Pacific

Cited by 45 publications

References 115 publications

Marine community metabolomes carry fingerprints of phytoplankton community composition

Marine community metabolomes carry fingerprints of phytoplankton community composition

Physical Forcing Controls the Basin‐Scale Occurrence of Nitrogen‐Fixing Organisms in the North Pacific Ocean

Unexpected presence of the nitrogen‐fixing symbiotic cyanobacterium UCYN‐A in Monterey Bay, California

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