ALBERT

Description: Microbial degradation of substrates to terminal products is commonly understood as a unidirectional process. In individual enzymatic reactions, however, reversibility (reverse reaction and product back flux) is common. Hence, it is possible that entire pathways of microbial degradation are associated with back flux from the accumulating product pool through intracellular intermediates into the substrate pool. We investigated carbon and sulfur back flux during the anaerobic oxidation of methane (AOM) with sulfate, one of the least exergonic microbial catabolic processes known. The involved enzymes must operate not far from the thermodynamic equilibrium. Such an energetic situation is likely to favor product back flux. Indeed, cultures of highly enriched archaeal–bacterial consortia, performing net AOM with unlabeled methane and sulfate, converted label from 14C-bicarbonate and 35S-sulfide to 14C-methane and 35S-sulfate, respectively. Back fluxes reached 5% and 13%, respectively, of the net AOM rate. The existence of catabolic back fluxes in the reverse direction of net reactions has implications for biogeochemical isotope studies. In environments where biochemical processes are close to thermodynamic equilibrium, measured fluxes of labeled substrates to products are not equal to microbial net rates. Detection of a reaction in situ by labeling may not even indicate a net reaction occurring in the direction of label conversion but may reflect the reverse component of a so far unrecognized net reaction. Furthermore, the natural isotopic composition of the substrate and product pool will be determined by both the forward and back flux. This finding may have to be considered in the interpretation of stable isotope records.

Description: Among eukaryotes, four major phytoplankton lineages are responsible for marine photosynthesis; prymnesiophytes, alveolates, stramenopiles, and prasinophytes. Contributions by individual taxa, however, are not well known, and genomes have been analyzed fromonly the latter two lineages. Tiny "picoplanktonic" members of the prymnesiophyte lineage have long been inferred to be ecologically important but remain poorly characterized. Here, we examine pico-prymnesiophyte evolutionary history and ecology using cultivation-independent methods. 18S rRNA gene analysis showed picoprymnesiophytes belonged to broadly distributed uncultivated taxa. Therefore, we used targeted metagenomics to analyze uncultured pico-prymnesiophytes sorted by flow cytometry from subtropical North Atlantic waters. The data reveal a composite nuclear-encoded gene repertoire with strong green-lineage affiliations, which contrasts with the evolutionary history indicated by the plastid genome. Measured pico-prymnesiophyte growth rates were rapid in this region, resulting in primary production contributions similar to the cyanobacterium Prochlorococcus. On average, pico-prymnesiophytes formed 25 of global picophytoplankton biomass, with differing contributions in five biogeographical provinces spanning tropical to subpolar systems. Elements likely contributing to success include high gene density and genes potentially involved in defense and nutrient uptake. Our findings have implications reaching beyond pico-prymnesiophytes, to the prasinophytes and stramenopiles. For example, prevalence of putative Ni-containing superoxide dismutases (SODs), instead of Fe-containing SODs, seems to be a common adaptation among eukaryotic phytoplankton for reducing Fe quotas in low-Fe modern oceans. Moreover, highly mosaic gene repertoires, although compositionally distinct for each major eukaryotic lineage, now seem to be an underlying facet of successful marine phytoplankton.

Description: Machine learning covers a large set of algorithms that can be trained to identify patterns in data. Thanks to the increase in the amount of data and computing power available, it has become pervasive across scientific disciplines. We first highlight why machine learning is needed in marine ecology. Then we provide a quick primer on machine learning techniques and vocabulary. We built a database of & SIM;1000 publications that implement such techniques to analyse marine ecology data. For various data types (images, optical spectra, acoustics, omics, geolocations, biogeochemical profiles, and satellite imagery), we present a historical perspective on applications that proved influential, can serve as templates for new work, or represent the diversity of approaches. Then, we illustrate how machine learning can be used to better understand ecological systems, by combining various sources of marine data. Through this coverage of the literature, we demonstrate an increase in the proportion of marine ecology studies that use machine learning, the pervasiveness of images as a data source, the dominance of machine learning for classification-type problems, and a shift towards deep learning for all data types. This overview is meant to guide researchers who wish to apply machine learning methods to their marine datasets.

Description: Knowledge of the range and chronology of historic trade and long-distance transport of natural resources is essential for determining the impacts of past human activities on marine environments. However, the specific biological sources of imported fauna are often difficult to identify, in particular if species have a wide spatial distribution and lack clear osteological or isotopic differentiation between populations. Here, we report that ancient fish-bone remains, despite being porous, brittle, and light, provide an excellent source of endogenous DNA (15–46%) of sufficient quality for whole-genome reconstruction. By comparing ancient sequence data to that of modern specimens, we determine the biological origin of 15 Viking Age (800–1066 CE) and subsequent medieval (1066–1280 CE) Atlantic cod (Gadus morhua) specimens from excavation sites in Germany, Norway, and the United Kingdom. Archaeological context indicates that one of these sites was a fishing settlement for the procurement of local catches, whereas the other localities were centers of trade. Fish from the trade sites show a mixed ancestry and are statistically differentiated from local fish populations. Moreover, Viking Age samples from Haithabu, Germany, are traced back to the North East Arctic Atlantic cod population that has supported the Lofoten fisheries of Norway for centuries. Our results resolve a long-standing controversial hypothesis and indicate that the marine resources of the North Atlantic Ocean were used to sustain an international demand for protein as far back as the Viking Age.

Description: The anaerobic oxidation of methane (AOM) is one of the major sinks of this substantial greenhouse gas in marine environments. Recent investigations have shown that diverse communities of anaerobic archaea and sulfate-reducing bacteria are involved in AOM. Most of the relevant archaea are assigned to two distinct phylogenetic clusters, ANME-1 and ANME-2. A suite of specific 13C-depleted lipids demonstrating the presence of consortia mediating AOM in fossil and recent environments has been established. Here we report on substantial differences in the lipid composition of microbial consortia sampled from distinct compartments of AOM-driven carbonate reefs growing in the northwestern Black Sea. Communities in which the dominant archaea are from the ANME-1 cluster yield internally cyclized tetraether lipids typical of thermophiles. Those in which ANME-2 archaea are dominant yield sn-2-hydroxyarchaeol accompanied by crocetane and crocetenes. The bacterial lipids from these communities are also distinct even though the sulfate-reducing bacteria all belong to the Desulfosarcina/Desulfococcus group. Nonisoprenoidal glycerol diethers are predominantly associated with ANME-1-dominated communities. Communities with ANME-2 yield mainly conventional, ester-linked diglycerides. ANME-1 archaea and associated sulfate-reducing bacteria seem to be enabled to use low concentrations of methane and to grow within a broad range of temperatures. Our results offer a tool for the study of recent and especially of fossil methane environments.

Description: Ammonia-oxidizing archaea are ubiquitous in marine and terrestrial environments and now thought to be significant contributors to carbon and nitrogen cycling. The isolation of Candidatus “Nitrosopumilus maritimus” strain SCM1 provided the opportunity for linking its chemolithotrophic physiology with a genomic inventory of the globally distributed archaea. Here we report the 1,645,259-bp closed genome of strain SCM1, revealing highly copper-dependent systems for ammonia oxidation and electron transport that are distinctly different from known ammonia-oxidizing bacteria. Consistent with in situ isotopic studies of marine archaea, the genome sequence indicates N. maritimus grows autotrophically using a variant of the 3-hydroxypropionate/4-hydroxybutryrate pathway for carbon assimilation, while maintaining limited capacity for assimilation of organic carbon. This unique instance of archaeal biosynthesis of the osmoprotectant ectoine and an unprecedented enrichment of multicopper oxidases, thioredoxin-like proteins, and transcriptional regulators points to an organism responsive to environmental cues and adapted to handling reactive copper and nitrogen species that likely derive from its distinctive biochemistry. The conservation of N. maritimus gene content and organization within marine metagenomes indicates that the unique physiology of these specialized oligophiles may play a significant role in the biogeochemical cycles of carbon and nitrogen.

Description: Archaea associated with marine sponges are active and influence the nitrogen metabolism of sponges. However, we know little about their occurrence, specificity, and persistence. We aimed to elucidate the relative importance of host specificity and biogeographic background in shaping the symbiotic archaeal communities. We investigated these communities in sympatric sponges from the Mediterranean (Ircinia fasciculata and Ircinia oros, sampled in summer and winter) and from the Caribbean (Ircinia strobilina and Mycale laxissima). PCR cloning and sequencing of archaeal 16S rRNA and amoA genes showed that the archaeal community composition and structure were different from that in seawater and varied among sponge species. We found that the communities were dominated by ammonia-oxidizing archaea closely related to Nitrosopumilus. The community in M. laxissima differed from that in Ircinia spp., including the sympatric sponge I. strobilina; yet, geographical clusters within Ircinia spp. were observed. Whereas archaeal phylotypes in Ircinia spp. were persistent and belong to 'sponge-enriched' clusters, archaea in M. laxissima were closely related with those from diverse habitats (i.e. seawater and sediments). For all four sponge species, the expression of the archaeal amoA gene was confirmed. Our results indicate that host-specific processes, such as host ecological strategy and evolutionary history, control the sponge-archaeal communities.

Description: The ability of microorganisms to withstand long periods with extremely low energy input has gained increasing scientific attention in recent years. Starvation experiments in the laboratory have shown that a phylogenetically wide range of microorganisms evolve fitness-enhancing genetic traits within weeks of incubation under low-energy stress. Studies on natural environments that are cut off from new energy supplies over geologic time scales, such as deeply buried sediments, suggest that similar adaptations might mediate survival under energy limitation in the environment. Yet, the extent to which laboratory-based evidence of starvation survival in pure or mixed cultures can be extrapolated to sustained microbial ecosystems in nature remains unclear. In this review, we discuss past investigations on microbial energy requirements and adaptations to energy limitation, identify gaps in our current knowledge, and outline possible future foci of research on life under extreme energy limitation.

Description: Calcifying echinoid larvae respond to changes in seawater carbonate chemistry with reduced growth and developmental delay. To date, no information exists on how ocean acidification acts on pH homeostasis in echinoderm larvae. Understanding acid–base regulatory capacities is important because intracellular formation and maintenance of the calcium carbonate skeleton is dependent on pH homeostasis. Using H+-selective microelectrodes and the pH-sensitive fluorescent dye BCECF, we conducted in vivo measurements of extracellular and intracellular pH (pHe and pHi) in echinoderm larvae. We exposed pluteus larvae to a range of seawater CO2 conditions and demonstrated that the extracellular compartment surrounding the calcifying primary mesenchyme cells (PMCs) conforms to the surrounding seawater with respect to pH during exposure to elevated seawater pCO2. Using FITC dextran conjugates, we demonstrate that sea urchin larvae have a leaky integument. PMCs and spicules are therefore directly exposed to strong changes in pHe whenever seawater pH changes. However, measurements of pHi demonstrated that PMCs are able to fully compensate an induced intracellular acidosis. This was highly dependent on Na+ and HCO3−, suggesting a bicarbonate buffer mechanism involving secondary active Na+-dependent membrane transport proteins. We suggest that, under ocean acidification, maintained pHi enables calcification to proceed despite decreased pHe. However, this probably causes enhanced costs. Increased costs for calcification or cellular homeostasis can be one of the main factors leading to modifications in energy partitioning, which then impacts growth and, ultimately, results in increased mortality of echinoid larvae during the pelagic life stage.

Description: Coccolithophores are an important component of the Earth system, and, as calcifiers, their possible susceptibility to ocean acidification is of major concern. Laboratory studies at enhanced pCO2 levels have produced divergent results without overall consensus. However, it has been predicted from these studies that, although calcification may not be depressed in all species, acidification will produce "a transition in dominance from more to less heavily calcified coccolithophores"Ridgwell A, et al., (2009) Biogeosciences 6:2611-2623. A recent observational study Beaufort L, et al., (2011) Nature 476:80-83 also suggested that coccolithophores are less calcified in more acidic conditions.We present the results of a large observational study of coccolithophore morphology in the Bay of Biscay. Samples were collected once a month for over a year, along a 1,000-km-long transect. Our data clearly show that there is a pronounced seasonality in the morphotypes of Emiliania huxleyi, the most abundant coccolithophore species. Whereas pH and CaCO 3saturation are lowest in winter, the E. huxleyi population shifts from 〈10% (summer) to >90% (winter) of the heavily calcified form. However, it is unlikely that the shifts in carbonate chemistry alone caused the morphotype shift. Our finding that the most heavily calcified morphotype dominates when conditions are most acidic is contrary to the earlier predictions and raises further questions about the fate of coccolithophores in a high-CO2 world.