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Untangling microbial evolution in the oceans: How the interaction of biological and physical timescales determine marine microbial evolutionary strategies

Posted by mmaheigan

· Wednesday, March 11th, 2020

Marine microbes are the engines of global biogeochemical cycling in the oceans. They are responsible for approximately half of all photosynthesis on the planet and drive the ‘biological pump’, which transfers organic carbon from the surface to the deep ocean. As such, it is important to determine how marine microbes will adapt and evolve in response to a changing climate in order to understand and predict how the global carbon cycle may change. However, we still lack a mechanistic understanding of how and how fast microorganisms adapt to stressful and changing environments. This is particularly challenging due to the diversity of organisms that live in the ocean and the dynamic nature of the oceans themselves—microbes are at the whim of ocean currents and so get transported large distances fairly quickly. For the first time, a new study published in PNAS provides a prediction on the controls of microbial evolutionary timescales in the oceans. The authors hypothesize that there is a trade-off for marine microbes between ability to evolve to long-term changes versus respond to shorter term variability. Their results suggest that marine microbes commonly experience conditions that favor a short-term strategy at the cost of long-term adaptation. This trade-off determines evolutionary timescales and provides a foundation for understanding distributions of microbial traits and biogeochemistry.

Illustration of trade-off in evolutionary strategy as a function of environmental variability. Trajectories where individuals perceived high environmental variability (a & b) exhibited low selective pressure for any one environment but allowed for high environmental tracking. Trajectories where individuals perceived a more stable environment (c&d) had high selective pressure for ’new environments’ (high probability of a selective sweep) but these individuals exhibited poor environmental tracking. Panels a and c show trajectories where selective sweeps were highly probable (red), likely (yellow), and had a low probability (grey). Panels b and d show the estimated persistence of non-genetic modifications necessary for environmental tracking, where grey indicates unrealistically long timescales.

Authors:
Nathan G. Walworth (University of Southern California)
Emily J. Zakem (University of Southern California)
John P. Dunne (Geophysical Fluid Dynamics Laboratory, NOAA)
Sinéad Collins (University of Edinburgh)
Naomi M. Levine (University of Southern California)

Diatoms commit iron piracy with stolen bacterial gene

Posted by mmaheigan

· Tuesday, February 4th, 2020

Since diatoms carry out much of the primary production in iron-limited marine environments, constraining the details of how these phytoplankton acquire the iron they need is paramount to our understanding of biogeochemical cycles of iron-depleted high-nutrient low-chlorophyll (HNLC) regions. The proteins involved in this process are largely unknown, but McQuaid et al. (2018) scientists described a carbonate-dependent uptake protein that enables diatoms to access inorganic iron dissolved in seawater. As increasing atmospheric CO₂ results in decreased seawater carbonate ion concentrations, this iron uptake strategy may have an uncertain future. In a recent study published in PNAS, authors used CRISPR technology to characterize a parallel uptake system that requires no carbonate and is therefore not impacted by ocean acidification.

This system targets an organically complexed form of iron (siderophores, molecules that bind and transport iron in microorganisms) that is only produced by co-occurring microbes. Two genes are required to convert siderophores from a potent toxicant to an essential nutrient. One of these (FBP1) is a receptor that was horizontally acquired from siderophore-producing bacteria. The other (FRE2) is a eukaryotic reductase that facilitates the dissociation of Fe-siderophore complexes.

Figure caption: (A) Growth curves of diatom cultures ( • = WT, ◇ = ΔFBP1, ☐ = ΔFRE2) in low iron media. (B) Growth in same media with siderophores added. (C) Diatoms under 1000x magnification, brightfield. (D) mCherry-FBP1. (E) Plastid autofluorescence. (F) YFP-FRE2. (G) Phylogenetic tree of FBP1 and related homologs.

Are diatoms really stealing siderophores from hapless bacteria? The true nature of this interaction is unknown and may at times be mutualistic. For example, when iron availability limits the carbon supply to a microbial community, heterotrophic bacteria may benefit from using siderophores to divert iron to diatom companions. Further work is needed to understand the true ecological basis for this interaction, but these results suggest that as long as diatoms and bacteria co-occur, iron limitation in marine ecosystems will not be exacerbated by ocean acidification.

Authors:
Tyler Coale (Scripps Institution of Oceanography, J.Craig Venter Institute)
Mark Moosburner (Scripps Institution of Oceanography, J.Craig Venter Institute)
Aleš Horák (Biology Centre CAS, Institute of Parasitology, University of South Bohemia)
Miroslav Oborník (Biology Centre CAS, Institute of Parasitology, University of South Bohemia)
Katherine Barbeau (Scripps Institution of Oceanography)
Andrew Allen (Scripps Institution of Oceanography, J.Craig Venter Institute)

Also see joint post on the GEOTRACES website

Unexpected DOC additions in the deep Atlantic

Posted by mmaheigan

· Tuesday, January 7th, 2020

Oceanic dissolved organic carbon (DOC) ultimately exchanges with atmospheric CO₂ and thus represents an important carbon source/sink with consequence for climate. Most of the DOC is recalcitrant to microbial degradation, with some fractions surviving for thousands of years. Therefore, DOC in the deep ocean was thought to be stable or to decrease slowly over decades to centuries due to biotic and abiotic sinks. However, a study published in Global Biogeochemical Cycles shows that there are some zones of the deep Atlantic Ocean where recalcitrant DOC experiences net production. Using data from oceanographic cruises across the Atlantic Ocean, the authors first identified the major water masses in the basin and the percentage of each in every sample taken for DOC analysis. The study revealed net additions of 27 million tons of dissolved organic carbon per year in the deep South Atlantic. On the other hand, the North Atlantic serves as a net sink, removing 298 million tons of carbon annually. DOC production observed in the deep Atlantic is probably due to the sinking particles that solubilize into DOC, since DOC enrichment was most evident at latitudes characterized as elevated productivity divergence zones.

Figure 1. Water masses along GO-SHIP line A16 (colored dots) and recalcitrant DOC variations due to biogeochemical processes (black dots within each water mass) in the deep Atlantic Ocean. Water mass domains are defined as the set of samples with the corresponding water mass proportion ≥50%. Recalcitrant DOC latitudinal variations per water stratum due to biogeochemical processes (ΔDOC) is in μmol kg^-1. Numbers on the plots are DOC values for the corresponding dots. Scales (not shown) are the same for all the plots, from -4 to 6 μmol kg^-1. Positive (negative) ΔDOC indicates values higher (lower) than the average DOC calculated for each water mass using an optimum multiparameter (OMP) analysis. DOC = dissolved organic carbon. AAIW = Antarctic Intermediate Water; UNADW = upper North Atlantic Deep Water; ISOW = Iceland Scotland Overflow Water; CDW = Circumpolar Deep Water; WSDW = Weddell Sea Deep Water. Figure created with Ocean Data View (Schlitzer, 2015).

Considering that the net DOC production over the entire Atlantic basin euphotic zone is 0.70–0.75 Pg C year^-1, the authors estimated that 30–39% of that DOC is consumed in the deep Atlantic subsequent to its export by overturning circulation. The upper North Atlantic Deep Water (UNADW) acts as the primary sink, accounting for 66% of the recalcitrant DOC removal in the North Atlantic. Conversely, the Antarctic Intermediate Water (AAIW) is the primary recipient, with 45% of recalcitrant DOC production in the South Atlantic, closely followed by the old UNADW that gains 44% of the recalcitrant DOC in the southern basin.

The Atlantic works as a mosaic of water masses, where both removal and addition of recalcitrant DOC occurs, with the dominant term dependent on the origin, temperature, age and depth of the water masses. The production of recalcitrant DOC in the deep ocean should be considered in biogeochemical models dealing with the carbon cycle and climate.

Authors:
C. Romera-Castillo and J. L. Pelegrí (Instituto de Ciencias del Mar, CSIC, Spain)
M. Álvarez (Instituto Español de Oceanografía, Spain)
D. A. Hansell (University of Miami, USA)
X. A. Álvarez-Salgado (Instituto de Investigaciones Marinas, CSIC, Spain)

Ocean microbes drive fluctuating nutrient loss

Posted by mmaheigan

· Tuesday, May 28th, 2019

The removal of bioavailable nitrogen (N) by anaerobic microbes in the ocean’s oxygen deficient zones (ODZs) is thought to vary over time primarily as a result of climate impacts on ocean circulation and primary production. However, a recent study in PNAS using a data-constrained model of the microbial ecosystem in the world’s largest ODZ revealed that internal species oscillations cause local- to basin-scale fluctuations in the rate of N loss, even in a completely stable physical environment. Such ecosystem oscillations have been hypothesized for nearly a century in idealized models, but are rarely shown to persist in a three-dimensional ocean circulation model.

Figure caption. Ecological variability in the basin-scale rate of nitrogen loss over time (left) and in the local-scale contribution of autotrophic anammox to total N loss (right) in a model with unchanging ocean circulation. In the left panel, colors represent model simulations with different biological parameters. In the right panel, colors represent distinct locations within the ODZ in the standard model simulation.

These emergent ecosystem dynamics arise at the oxic-anoxic interface from O₂-dependent resource competition between aerobic and anaerobic microbes, and leave a unique geochemical fingerprint: infrequent spikes in ammonium that are observable in nutrient measurements from the ODZ. Non-equilibrium ecosystem behavior driven by competition among aerobic nitrifiers, anaerobic denitrifiers, and anammox bacteria also generates fluctuations in the balance of autotrophic versus heterotrophic N loss pathways that help reconcile conflicting field observations.

These internally driven fluctuations in microbial community structure partially obscure a direct correspondence between the chemical environment and microbial rates, a universal assumption in biogeochemical models. Because of the fundamental nature of the underlying mechanism, similar dynamics are hypothesized to occur across wide-ranging microbial communities in diverse habitats.

Authors:
Justin L. Penn (University of Washington)
Thomas Weber (University of Rochester),
Bonnie X. Chang (University of Washington, NOAA)
Curtis Deutsch (University of Washington)

See also the OCB2019 plenary session: Anthropogenic changes in ocean oxygen: Coastal and open ocean perspectives (Monday, June 24, 2019)

Microbes: Gatekeepers of earth’s deep carbon?

Posted by mmaheigan

· Tuesday, May 14th, 2019

In 2017, an interdisciplinary group of early career scientists, the Biology Meets Subduction team, visited Costa Rica’s subduction zone, where the ocean floor sinks beneath the continent, to find out if subterranean microbes affect geological processes that move carbon from Earth’s surface into the deep interior.

Using carbon and helium isotope measurements of water and nearby sediments from geothermal springs in northern and central Costa Rica, the study published recently in Nature demonstrated that microbes consume and trap a small but measurable amount of the carbon sinking into the trench off Costa Rica’s Pacific coast. The microbes may also be involved in chemical processes that pull out even more carbon, leaving cement-like veins of calcite in the crust.

Figure 1: Schematic of deep carbon cycle subduction at the forearc region and into the mantle.

The team discovered that low temperatures in the forearc support microbial life and water-rock interactions that divert the down-going carbon from the subducting slab and trap it in the crust. The study estimates that about 94 percent of that redirected carbon transforms into calcite minerals and microbial biomass.

Figure 2: Biofilm in a natural seep in Costa Rica. Credit: Peter Barry.

These unexpected findings have important implications for how much carbon moves from Earth’s surface into the interior, especially over geological timescales. If these biological and geochemical processes occur worldwide, they would translate to 19% less carbon entering the deep mantle than previously estimated.

Authors:
PH Barry
JM de Moor
D Giovannelli
M Schrenk
D Hummer
T Lopez
CA Pratt
Y Alpízar Segura
A Battaglia
P Beaudry
G Bini
M Cascante
G d’Errico

M di Carl
D Fattorini
K Fullerton
E Gazel
G González
SA Halldórsson
K Iacovino
JT Kulongoski
E Manini
M Martínez
H Miller
M Nakagawa
S Ono

S Patwardhan
CJ Ramírez
F Regoli
F Smedile
S Turner
C Vetriani
M Yücel
CJ Ballentine
TP Fischer
DR Hilton
KG Lloyd

Physics shed new light on microbial filter-feeding

Posted by mmaheigan

· Wednesday, September 26th, 2018

Microbial filter-feeders actively filter water for bacteria-sized prey, but hydrodynamic theory predicts that their filtration rate should be one order of magnitude lower than what they realize. What is missing in our knowledge and modeling of these key components of aquatic food webs?

In a recent study published in PNAS, Nielsen et al. (2017) used a combination of microscopy observations, particle tracking, and analytical and computational fluid dynamics (CFD) to shed light on the physics of microbial filter-feeding. They found that analytical and computational fluid dynamic estimates agree that the observed filtration rate cannot be realized given the known morphology and flagellum kinematics. The estimates consistently fall one order of magnitude short of observed filtration rates. This led the authors to suggest that their study organism, the choanoflagellate Diaphanoeca grandis, has a so-called ‘flagellar vane’, a sheet-like extension of the flagellum seen in some members of the choanoflagellate sister group, the marine sponges. This structure would fundamentally change the physics of the filtration process, and the authors found that both the analytical and the computational estimates match observed filtration rates when such a structure is included.

Left: Choanoflagellate model morphology showing the protoplast (cell) in orange, the filter comprised of microvilli (black), the lorica and chimney (red) and the flagellum with vane (blue). Right: Experimentally observed near-cell flow field vs. flow field modelled using computational fluid dynamics including a flagellar vane. The filter cross-section is here shown in green. The modelled flow field provides a good match with the observed flow field. Without a flagellar vane, the model flow field is at least an order of magnitude weaker. This leads to the suggestion that a flagellar vane is needed to account for the observed flow field and clearance rate.

The new insights allow the authors to generalize about the trade-offs involved in microbial filtering, which is important to our understanding of the microbial loop in planktonic food webs. The results are of even wider interest since choanoflagellates are believed to be the evolutionary ancestors of all multicellular animals, many of which include cells that are fundamentally identical to choanoflagellates (e.g., the simple cuboidal epithelium cells of kidneys). Thus, microscale filtering not only happens in every single drop of seawater, it also happens inside most animals.

Learn more here.

Authors:
Lasse Tor Nielsen (National Institute of Aquatic Resources and Centre for Ocean Life, Technical University of Denmark)
Seyed Saeed Asadzadeh (Department of Mechanical Engineering, Technical University of Denmark)
Julia Dölger (Department of Physics and Centre for Ocean Life, Technical University of Denmark)
Jens H. Walther (Department of Mechanical Engineering, Technical University of Denmark, Denmark and Swiss Federal Institute of Technology Zürich, ETH Zentrum)
Thomas Kiørboe (National Institute of Aquatic Resources and Centre for Ocean Life, Technical University of Denmark)
Anders Andersen (Department of Physics and Centre for Ocean Life, Technical University of Denmark)

The sea surface microlayer in a future ocean

Posted by mmaheigan

· Tuesday, November 28th, 2017

The sea surface microlayer (SML) is the boundary interface between the atmosphere and ocean, spanning the uppermost ~1 mm of the ocean. Covering 70% of the Earth’s surface, the SML supports a rich diversity of life, serving as an incubator for eggs and larvae. The SML controls air-sea interactions and serves as an important hotspot of microbially mediated biochemical activity. A recent review paper by Wurl et al. highlights the important role of the SML in climate and ecosystem function and how it might change in the future.

Figure Caption: The sea surface microlayer comprises a complex biofilm and serves as a biochemical micro-reactor with distinct microbial communities and short-term carbon accumulation.

The SML is directly exposed to meteorological forces such as UV radiation, precipitation, and diurnal warming. Since these forces will be impacted by climate change, the SML is also likely to experience changes in the future. For example, projected increases in primary productivity in the upper sunlit layer of the ocean may enhance the supply of surface-active organic material to the SML with accompanying feedbacks on the molecular diffusion and conduction processes that drive exchange of heat and climate-relevant gases such as CO₂ between the ocean and atmosphere. Furthermore, changes in UV flux may enhance the SML’s role as a biochemical reactor in which unique microbial communities and photochemical reactions occur, including the transformation of deposited atmospheric particles like dust into bioavailable nutrients like iron to fuel phytoplankton production. Increasing levels of manmade pollutants such as pharmaceuticals and micro-plastics are accumulating in the SML. These and other pollutants have the potential to disrupt biochemical and photochemical processes in the SML, as well as the unique and diverse food webs it supports.

Moving forward, novel techniques and a holistic approach will be needed to improve our understanding of highly complex SML dynamics. Multidisciplinary data sets that link microbial community structure and function with biogeochemistry will be needed, and eventually, the SML should be included in computer models used to forecast future changes in climate, marine ecosystems, and biogeochemistry.

Authors:
Oliver Wurl (Carl von Ossietzky Universität Oldenburg, Institute for Chemistry and Biology of the Marine Environment)
Werner Ekau (Leibniz Centre for Tropical Marine Research, Bremen)
William M. Landing (Florida State University, Department of Earth, Ocean, and Atmospheric Science)
Christopher J. Zappa (Lamont-Doherty Earth Observatory, Columbia University)

The Ross Sea deep microbial community’s role in sequestering CO2

Posted by mmaheigan

· Thursday, November 9th, 2017

Antarctic shelf systems generate the densest waters in the world. These shelf waters are the building blocks of Antarctic Bottom Water, the ocean’s abyssal water mass. These bottom waters have the potential to sequester carbon out of the atmosphere for millennia. One such form of marine carbon is dissolved organic carbon (DOC). DOC is produced in the surface ocean via primary production and is the global ocean’s largest standing stock of reduced carbon.

In a recent study, Bercovici et al (2017) used hydrographic and biogeochemical measurements to assess the mechanism that brings DOC into the shelf waters of the Ross Sea, the shelf system in the Pacific sector of Antarctica. These mechanisms include sinking particles, brine rejection caused by katabatic winds in the Terra Nova Bay polynya, and vertical mixing. This study revealed that DOC is primarily introduced into the deeper shelf waters via convective overturning and deep vertical mixing upon the onset of austral winter. Substantial DOC enrichment of shelf waters suggests that this carbon is exported off the shelf into Antarctic Bottom Water. However, this study finds much of the excess Ross Sea shelf DOC is actually consumed and remineralized to CO₂ by deep microbial communities at the slope of the Ross Sea shelf, ultimately sequestering this carbon into the ocean’s interior.

Physical and biological processes have the potential to introduce carbon into the dense shelf waters (blue) in the Ross Sea. Incoming waters (yellow) are modified from the Southern Ocean’s circumpolar waters. At the onset of winter, cooler temperatures and katabatic winds cause brine rejection. The rejection of brine, sinking particles and vertical mixing are all potential mechanisms for bringing DOC to the dense shelf waters. At the shelf slope, outflowing shelf waters ultimately contribute to Antarctic Bottom Water formation. This research furthers our understanding of global carbon cycling through demonstrating that Antarctic shelf systems have the potential to sequester organic carbon into the abyssal ocean.

Authors:
Sarah K. Bercovici (Rosenstiel School of Marine and Atmospheric Science, University of Miami)
Bruce A. Huber (Lamont Doherty Earth Observatory, Columbia University)
Hans B. Dejong (Stanford University)
Robert B. Dunbar (Stanford University)
Dennis A. Hansell (Rosenstiel School of Marine and Atmospheric Science, University of Miami)

Role for iron in controlling microbial phosphorus acquisition in the ocean

Posted by mmaheigan

· Thursday, October 12th, 2017

In the subtropical North Atlantic, dissolved inorganic phosphorus (DIP) concentrations are depleted and might co-limit N₂ fixation and microbial productivity. There are relatively large pools of dissolved organic phosphorus (DOP), but microbes need an enzyme to access this P source. One such alkaline phosphatase (APase) enzyme requires zinc (Zn) as its activating cofactor. This has been known for almost 30 years. However, recent crystallography studies revealed that two other widespread APase enzymes contain Fe. Via this requirement, Fe availability could regulate microbial access to the DOP pool.

As detailed in a recent publication in Nature Communications (Browning et al. 2017), this hypothesis was tested on a cruise across the tropical North Atlantic by adding Fe and Zn to incubated seawater and monitoring changes in bulk APase using a simple fluorescence assay. Adding Fe significantly increased APase activity in seawater samples collected in areas that were far-removed from coastal and aerosol Fe sources. Despite seawater Zn concentrations being much lower than Fe, it appeared not to be limiting.

Iron (Fe) and zinc (Zn) enrichment experiments conducted in the DIP-depleted tropical North Atlantic suggested that Fe, not Zn, could limit alkaline phosphatase activity (APA). DIP*=DIP–DIN/16, and represents excess DIP availability assuming a 16-fold higher microbial N requirement. Results in the bar chart represent a subset of treatments from one experiment (out of eight conducted).

DIP is depleted in surface waters of the tropical North Atlantic because inputs of North African aerosol Fe stimulates N₂ fixation and leads to microbial drawdown of DIP. If the modern ocean is a good analog for the past, the lack of APase stimulation following experimental Zn addition could reflect limited evolutionary selection for Zn-containing APase. In general, DIP is only substantially depleted where there is enhanced Fe input fueling N₂ fixation; it therefore follows that any significant requirement for APases might be restricted to these relatively high-Fe, low-Zn waters.

On a shorter timescale, growing anthropogenic nitrogen input to the ocean relative to phosphorus could result in more prevalent oceanic phosphorus deficiency. Corresponding iron inputs might then serve as an important control on phosphorus availability for microbes in these regions.

Authors:

Tom Browning (GEOMAR Helmholtz Centre for Ocean Research, Kiel, Germany)
Eric Achterberg (GEOMAR)
Jaw Chuen Yong (GEOMAR)
Insa Rapp (GEOMAR)
Caroline Utermann (GEOMAR)
Anja Engel (GEOMAR)
Mark Moore (Ocean and Earth Science, University of Southampton, Southampton, UK)

Sinking particles as biogeochemical hubs for trace metal cycling and release

Posted by mmaheigan

· Thursday, September 14th, 2017

The extent to which the return of major and minor elements to the dissolved phase in the deep ocean (termed remineralization) is decoupled plays a major role in setting patterns of nutrient limitation in the global ocean. It is well established that major elements such as phosphorus, silicon, and carbon are released at different rates from sinking particles, with major implications for nutrient recycling. Is this also the case for trace metals?

A recent publication by Boyd et al. in Nature Geoscience provides new insights into the biotic and abiotic processes that drive remineralization of metals in the ocean. Particle composition changes rapidly with depth with both physical (disaggregation) and biogeochemical (grazing; desorption) processes leading to a marked decrease in the total surface area of the particle population. The proportion of lithogenic metals in sinking particles also appears to increase with depth, as the biogenic metals may be more labile and hence more readily removed.

Findings from GEOTRACES process studies revealed that release rates for trace elements such as iron, nickel, and zinc vary from each other. Microbes play a key role in determining the turnover rates for nutrients and trace elements. Decoupling of trace metal recycling in the surface ocean and below may result from their preferential removal by microbes to satisfy their nutritional requirements. In addition, the chemistry operating on particle surfaces plays a pivotal role in determining the specific fates of each trace metal. Teasing apart these factors will take time, as there is a complex interplay between chemical and biological processes. Improving our understanding is crucial, as these processes are not currently well represented by state-of-the-art ocean biogeochemical models.

Figure caption: Rapid changes in the characteristics of sinking particles over the upper 200 m as evidenced by: a) differential release of trace metals from sinking diatoms; b) changes in proportion of lithogenic versus biogenic materials; and c) ten-fold decrease in total particle surface area.

Authors:
Philip Boyd (IMAS, Australia)
Michael Ellwood (ANU, Australia)
Alessandro Tagliabue (Liverpool, UK)
Ben Twining (Bigelow, USA)

Relevant links:
GEOTRACES Digest: Iron Superstar

Joint workshop with GEOTRACES in August 2016: Biogeochemical Cycling of Trace Elements within the Ocean

Funding for the Ocean Carbon & Biogeochemistry Project Office is provided by the National Science Foundation (NSF) and the National Aeronautics and Space Administration (NASA). The OCB Project Office is housed at the Woods Hole Oceanographic Institution.

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