Marine Biological Laboratory
  • Falmouth, MA, United States
Recent publications
Agricultural decision-making by different interest groups (e.g., farmers, development agents and policy makers) usually takes place on different scales (e.g., plot, landscape and country). Currently, tools to assist decision-making are either dedicated to small-scale management guidance or large-scale assessment, which ignore the cross-scale linkages and interactions and thus may not provide robust and consistent guidance and assessment. Here, we developed an advanced agricultural modeling framework by integrating the strengths of conventional crop models in representing crop growth processes and management practices into a terrestrial biosphere model (TBM), the Dynamic Land Ecosystem Model (DLEM), to meet the cross-scale application needs (e.g., adaptation and mitigation). Specifically, dynamic crop growth processes, including crop-specific phenological development, carbon allocation, yield formation, biological nitrogen fixation processes, and management practices such as tillage, cover cropping and genetic improvements, were explicitly represented in DLEM. The new model was evaluated against site-scale observations and the results showed that the model performed generally well, with an average normalized root mean square error of 19.91% for leaf area index and 17.46% for aboveground biomass at the seasonal scale and 14.42% for annual yield. Then the model was applied to simulate corn, soybean, and winter wheat productions in the conterminous United States from 1960 to 2018. The spatial patterns of simulated crop productions were consistent with ground survey data. Our model also captured both the long-term trends and interannual variations of the total national productions of the three crops. This study demonstrates the significance of fusing conventional crop modeling techniques into TBMs to establish a unified modeling framework, which holds the potential to address climate impacts, adaptation and mitigation across varied spatiotemporal scales.
In Brazilian marine ecosystems, Farfantepenaeus brasiliensis and F. paulensis are caught around 40-meter isobath, whereas in shallower waters (<20 m), juveniles are caught as bycatch in fisheries targeting other shrimp species. Despite their importance in fisheries, the ecology of the two Farfantepenaeus species is not well understood. Their recruitment patterns still are not clear and both species in adult phase are landed as pink shrimp, making evaluations impossible. In this study, we focused on evaluating a 23-year fisheries-independent dataset, seeking to clarify recruitment patterns and to relate them to El Niño Southern Oscillation events and environmental factors in the Ubatuba Bay, a traditional trawling area in Southeast Brazil. Generalized Additive Models indicated that both species shared some patterns in early life stages, being more abundant between January to April, when granulometry presented Phi ≤ 4.5, and salinities and temperatures are higher than 35 and 25 ºC, respectively. Also F. paulensis abundance increased under El Niño events. The higher capture of Farfantepenaeus spp. in a period with intense trawling activity and prior to the closed season (March to May) indicated that populations are not adequately protected in the study area. Beyond highlighting the role of shallow marine areas as potential nursery ecosystems for species of pink shrimp, these results provide evidence to support the fishing closed season in the southeastern and southern regions of Brazil.
Background The human mouth is a natural laboratory for studying how bacterial communities differ across habitats. Different bacteria colonize different surfaces in the mouth—teeth, tongue dorsum, and keratinized and non-keratinized epithelia—despite the short physical distance between these habitats and their connection through saliva. We sought to determine whether more tightly defined microhabitats might have more tightly defined sets of resident bacteria. A microhabitat may be characterized, for example, as the space adjacent to a particular species of bacterium. Corncob structures of dental plaque, consisting of coccoid bacteria bound to filaments of Corynebacterium cells, present an opportunity to analyze the community structure of one such well-defined microhabitat within a complex natural biofilm. Here, we investigate by fluorescence in situ hybridization and spectral imaging the composition of the cocci decorating the filaments. Results The range of taxa observed in corncobs was limited to a small subset of the taxa present in dental plaque. Among four major groups of dental plaque streptococci, two were the major constituents of corncobs, including one that was the most abundant Streptococcus species in corncobs despite being relatively rare in dental plaque overall. Images showed both Streptococcus types in corncobs in all individual donors, suggesting that the taxa have different ecological roles or that mechanisms exist for stabilizing the persistence of functionally redundant taxa in the population. Direct taxon-taxon interactions were observed not only between the Streptococcus cells and the central corncob filament but also between Streptococcus cells and the limited subset of other plaque bacteria detected in the corncobs, indicating species ensembles involving these taxa as well. Conclusions The spatial organization we observed in corncobs suggests that each of the microbial participants can interact with multiple, albeit limited, potential partners, a feature that may encourage the long-term stability of the community. Additionally, our results suggest the general principle that a precisely defined microhabitat will be inhabited by a small and well-defined set of microbial taxa. Thus, our results are important for understanding the structure and organizing principles of natural biofilms and lay the groundwork for future work to modulate and control biofilms for human health.
The remarkable regenerative abilities of the small cnidarian Hydra vulgaris include the capacity to reassemble itself after dissociation into individual cells. Here, we present a robust protocol for the dissociation and reaggregation of Hydra tissue that addresses many common challenges encountered during the preparation and execution of the dissociation, as well as the formation and care of regenerating cellular aggregates. Analysis of the process provides insight into the mechanisms of nervous system self-organization. For complete details on the use and execution of this protocol, please refer to Lovas and Yuste (2021).
A detailed understanding of where bacteria localize is necessary to advance microbial ecology and microbiome‐based therapeutics. The site‐specialist hypothesis predicts that most microbes in the human oral cavity have a primary habitat type within the mouth where they are most abundant. We asked whether this hypothesis accurately describes the distribution of the members of the genus Streptococcus, a clinically relevant taxon that dominates most oral sites. Prior analysis of 16S rRNA gene sequencing data indicated that some oral Streptococcus clades are site‐specialists while others may be generalists. However, within complex microbial populations composed of numerous closely related species and strains, such as the oral streptococci, genome‐scale analysis is necessary to provide the resolution to discriminate closely related taxa with distinct functional roles. Here we assess whether individual species within this genus are specialists using publicly available genomic sequence data that provides species‐level resolution. We chose a set of high‐quality representative genomes for human oral Streptococcus species. Onto these genomes, we mapped shotgun metagenomic sequencing reads from supragingival plaque, tongue dorsum, and other sites in the oral cavity. We found that every abundant Streptococcus species in the healthy human oral cavity showed strong site tropism and that even closely related species such as S. mitis, S. oralis, and S. infantis specialized in different sites. These findings indicate that closely related bacteria can have distinct habitat distributions in the absence of dispersal limitation and under similar environmental conditions and immune regimes. Substantial overlap between the core genes of these three species suggests that site‐specialization is determined by subtle differences in genomic content. This article is protected by copyright. All rights reserved
Long-term observations and experiments in diverse drylands reveal how ecosystems and services are responding to climate change. To develop generalities about climate change impacts at dryland sites, we compared broadscale patterns in climate and synthesized primary production responses among the eight terrestrial, nonforested sites of the United States Long-Term Ecological Research (US LTER) Network located in temperate (Southwest and Midwest) and polar (Arctic and Antarctic) regions. All sites experienced warming in recent decades, whereas drought varied regionally with multidecadal phases. Multiple years of wet or dry conditions had larger effects than single years on primary production. Droughts, floods, and wildfires altered resource availability and restructured plant communities, with greater impacts on primary production than warming alone. During severe regional droughts, air pollution from wildfire and dust events peaked. Studies at US LTER drylands over more than 40 years demonstrate reciprocal links and feedbacks among dryland ecosystems, climate-driven disturbance events, and climate change.
The multiple biomarker approach is an effective tool to study the responses of aquatic organisms to contaminants. Summarizing multiple biomarker responses for facilitated communication of research findings has been aided by some integrated indices. Here we explain how existing integrated indices were built and why they turn out to be the wheel reinvented. We discuss the role of integrated indices in ecological risk assessment and recommend some changes in summarizing multiple biomarker results. This article is protected by copyright. All rights reserved.© 2022 The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC).
Kelps, seagrasses, and surfgrasses are ecosystem engineers on rocky shorelines, where they show remarkably high levels of primary production. Through analysis of their associated microbial communities, we found a variety of microbial metabolisms that may benefit the host, including nitrogen metabolisms, sulfur oxidation, and the production of B vitamins.
For the abundant marine Alphaproteobacterium Pelagibacter (SAR11), and other bacteria, phages are powerful forces of mortality. However, little is known about the most abundant Pelagiphages in nature, such as the widespread HTVC023P-type, which is currently represented by two cultured phages. Using viral metagenomic data sets and fluorescence-activated cell sorting, we recovered 80 complete, undescribed Podoviridae genomes that form 10 phylogenomically distinct clades (herein, named Clades I to X) related to the HTVC023P-type. These expanded the HTVC023P-type pan-genome by 15-fold and revealed 41 previously unknown auxiliary metabolic genes (AMGs) in this viral lineage. Numerous instances of partner-AMGs (colocated and involved in related functions) were observed, including partners in nucleotide metabolism, DNA hypermodification, and Curli biogenesis. The Type VIII secretion system (T8SS) responsible for Curli biogenesis was identified in nine genomes and expanded the repertoire of T8SS proteins reported thus far in viruses. Additionally, the identified T8SS gene cluster contained an iron-dependent regulator (FecR), as well as a histidine kinase and adenylate cyclase that can be implicated in T8SS function but are not within T8SS operons in bacteria. While T8SS are lacking in known Pelagibacter, they contribute to aggregation and biofilm formation in other bacteria. Phylogenetic reconstructions of partner-AMGs indicate derivation from cellular lineages with a more recent transfer between viral families. For example, homologs of all T8SS genes are present in syntenic regions of distant Myoviridae Pelagiphages, and they appear to have alphaproteobacterial origins with a later transfer between viral families. The results point to an unprecedented multipartner-AMG transfer between marine Myoviridae and Podoviridae. Together with the expansion of known metabolic functions, our studies provide new prospects for understanding the ecology and evolution of marine phages and their hosts. IMPORTANCE One of the most abundant and diverse marine bacterial groups is Pelagibacter. Phages have roles in shaping Pelagibacter ecology; however, several Pelagiphage lineages are represented by only a few genomes. This paucity of data from even the most widespread lineages has imposed limits on the understanding of the diversity of Pelagiphages and their impacts on hosts. Here, we report 80 complete genomes, assembled directly from environmental data, which are from undescribed Pelagiphages and render new insights into the manipulation of host metabolism during infection. Notably, the viruses have functionally related partner genes that appear to be transferred between distant viruses, including a suite that encode a secretion system which both brings a new functional capability to the host and is abundant in phages across the ocean. Together, these functions have important implications for phage evolution and for how Pelagiphage infection influences host biology in manners extending beyond canonical viral lysis and mortality.
The green seaweed Ulva is important from ecological and economic perspectives, but the identification of species is often problematic. Here we assessed and discussed different perspectives to establish a stable taxonomic framework for Ulva, which will benefit both ecological and applied research. We evaluated (1) the performance of commonly used DNA-barcode markers (ITS rDNA, rbcL, and tufA) using species delimitation methods (PTP and GMYC), (2) the usage of species names in the literature, and (3) the geographic coverage of genetic data to identify poorly sampled regions. Species delimitation employing the tufA gene was the most consistent across methods. Not surprisingly, DNA-based species delimitation was often in disagreement with traditional morphology-based species definitions. Biological species concepts, where tested, proved to be generally narrower than DNA-based species delimitation. Although the use of molecular markers has greatly improved our view of Ulva diversity, the names associated with DNA sequences in public databases are often unreliable, complicating species identification. Recently, sequencing type materials has considerably reduced the gap between DNA sequence data and Linnaean names, but our knowledge on Ulva diversity remains inadequate, especially in tropical regions. Perspectives for Ulva taxonomy include the consistent use of multiple DNA-barcode markers assisted by species delimitation methods, applications of genomic data, and crossing experiments. To arrive at a stable nomenclature, we outline the benefits and shortcomings of adhering to the rules and practices of the International Code of Nomenclature for algae, fungi, and plants, for example, by sequencing name-bearing types and discuss alternative approaches.
Structures made by scleractinian corals support diverse ocean ecosystems. Despite the importance of coral skeletons and their predicted vulnerability to climate change, few studies have examined the mechanical and crystallographic properties of coral skeletons at the micro- and nano-scales. Here, we investigated the interplay of crystallographic and microarchitectural organization with mechanical anisotropy within Porites skeletons by measuring Young’s modulus and hardness along surfaces transverse and longitudinal to the primary coral growth direction. We observed micro-scale anisotropy, where the transverse surface had greater Young’s modulus and hardness by ∼ 6 GPa and 0.2 GPa, respectively. Electron backscatter diffraction (EBSD) revealed that this surface also had a higher percentage of crystals oriented with the a-axis between ± 30-60∘, relative to the longitudinal surface, and a broader grain size distribution. Within a region containing a sharp microscale gradient in Young’s modulus, nanoscale indentation mapping, energy dispersive spectroscopy (EDS), EBSD, and Raman crystallography were performed. A correlative trend showed higher Young’s modulus and hardness in regions with individual crystal bases (c-axis) facing upward, and in crystal fibers relative to centers of calcification. These relationships highlight the difference in mechanical properties between scales (i.e. crystals, crystal bundles, grains). Observations of crystal orientation and mechanical properties suggest that anisotropy is driven by microscale organization and crystal packing, rather than intrinsic crystal anisotropy. In comparison with previous observations of nanoscale isotropy in corals, our results illustrate the role of hierarchical architecture in coral skeletons and the influence of biotic and abiotic factors on mechanical properties at different scales. Statement of significance Coral biomineralization and the ability of corals’ skeletal structure to withstand biotic and abiotic forces underpins the success of reef ecosystems. At the microscale, we show increased skeletal stiffness and hardness perpendicular to the coral growth direction. By comparing nano- and micro-scale indentation results, we also reveal an effect of hierarchical architecture on the mechanical properties of coral skeletons and hypothesize that crystal packing and orientation result in microscale anisotropy. In contrast to previous findings, we demonstrate that mechanical and crystallographic properties of coral skeletons can vary between surface planes, within surface planes, and at different analytical scales. These results improve our understanding of biomineralization and the effects of scale and direction on how biomineral structures respond to environmental stimuli.
Deimatic behaviours, also referred to as startle behaviours, are used against predators and rivals. Although many are spectacular, their proximate and ultimate causes remain unclear. In this review we aim to synthesise what is known about deimatic behaviour and identify knowledge gaps. We propose a working hypothesis for deimatic behaviour, and discuss the available evidence for the evolution, ontogeny, causation, and survival value of deimatic behaviour using Tinbergen's Four Questions as a framework. Our overarching aim is to direct future research by suggesting ways to address the most pressing questions in this field.
Honeybees use wide-field visual motion information to calculate the distance they have flown from the hive, and this information is communicated to conspecifics during the waggle dance. Seed treatment insecticides, including neonicotinoids and novel insecticides like sulfoxaflor, display detrimental effects on wild and managed bees, even when present at sublethal quantities. These effects include deficits in flight navigation and homing ability, and decreased survival of exposed worker bees. Neonicotinoid insecticides disrupt visual motion detection in the locust, resulting in impaired escape behaviors, but it had not previously been shown whether seed treatment insecticides disrupt wide-field motion detection in the honeybee. Here, we show that sublethal exposure to two commonly used insecticides, imidacloprid (a neonicotinoid) and sulfoxaflor, results in impaired optomotor behavior in the honeybee. This behavioral effect correlates with altered stress and detoxification gene expression in the brain. Exposure to sulfoxaflor led to sparse increases in neuronal apoptosis, localized primarily in the optic lobes, however there was no effect of imidacloprid. We propose that exposure to cholinergic insecticides disrupts the honeybee’s ability to accurately encode wide-field visual motion, resulting in impaired optomotor behaviors. These findings provide a novel explanation for previously described effects of neonicotinoid insecticides on navigation and link these effects to sulfoxaflor for which there is a gap in scientific knowledge.
Couplings between coastal watersheds and estuaries were assessed in a series of sites across SE New England. Nitrogen loads to watersheds increased during 1985–1996, but decreased afterwards due to lowered atmospheric deposition. Within-watershed nitrogen interception was high and linked to forest cover. Loads to estuaries also increased pre-1996 and decreased after because of lowered atmospheric inputs. Concentrations of nitrogen compounds were higher in estuaries subject to larger nitrogen loads from land. Estuarine nutrients showed large scatter and decreased from less-saline to saltier reaches. Chlorophyll concentrations were less reliable indicators of coupling to watershed loads. Water quality variables were lagging indicators of changing nitrogen loads, with shifts in concentrations becoming detectable several years after the 1996 shift in total nitrogen loads. Lag delays will be of significance for assessment of the effectiveness of estuarine water quality management.
Structural and mechanical properties of the decapod exoskeleton affect foraging, defense, and locomotion, making the ability of decapods to maintain their calcified exoskeleton a crucial physiological process. Ocean acidification (OA) poses a threat to marine biomes and their inhabitants, particularly calcifying organisms. Vulnerability of the snow crab, Chionecetes opilio, a commercially important, high-latitude species, to OA has not been explored. Although all oceans are experiencing acidification, abiotic factors in high-latitude areas increase the rate of acidification. We examined the effect of long-term (2-year) exposure to decreased seawater pH (7.8 and 7.5) on exoskeletal properties in post-terminal-molt female C. opilio. Since the effects of OA vary among body regions in decapods, exoskeletal properties (microhardness, thickness, and elemental composition) were measured in five body regions: the carapace, both claws, and both third-walking legs. Overall, the C. opilio exoskeleton was robust to OA in all body regions. Decreased pH had no effect on microhardness or thickness of the exoskeleton, despite a slight (~6%) reduction in calcium content in crabs held at pH 7.5. In contrast, exoskeletal properties varied dramatically among body regions regardless of pH. The exoskeleton of the claws was harder, thicker, and contained more calcium but less magnesium than that of other body regions. Exoskeleton of the legs was thinner than that of other body regions and contained significantly greater levels of magnesium (~2.5 times higher than the claws). Maintenance of exoskeletal properties after long-term OA exposure in C. opilio suggests that wild populations may tolerate future ocean pH conditions.
A breakdown in host-bacteria relationships has been associated with the progression of a number of marine diseases and subsequent mortality events. For the Pacific oyster, Crassostrea gigas, summer mortality syndrome (SMS) is one of the biggest constraints to the growth of the sector and is set to expand into temperate systems as ocean temperatures rise. Currently, a lack of understanding of natural spatiotemporal dynamics of the host-bacteria relationship limits our ability to develop microbially based monitoring approaches. Here, we characterised the associated bacterial community of C. gigas, at two Irish oyster farms, unaffected by SMS, over the course of a year. We found C. gigas harboured spatiotemporally variable bacterial communities that were distinct from bacterioplankton in surrounding seawater. Whilst the majority of bacteria-oyster associations were transient and highly variable, we observed clear patterns of stability in the form of a small core consisting of six persistent amplicon sequence variants (ASVs). This core made up a disproportionately large contribution to sample abundance (34 ± 0.14%), despite representing only 0.034% of species richness across the study, and has been associated with healthy oysters in other systems. Overall, our study demonstrates the consistent features of oyster bacterial communities across spatial and temporal scales and provides an ecologically meaningful baseline to track environmental change.
Although terrestrial hydrothermal systems are considered among the most fascinating environments, how their unique and extreme conditions can affect microorganisms selection and the role in biogeochemical cycles has not yet been well elucidated. A combined geochemical and microbiological exploration in waters and sediments from ten sampling points along a sharp temperature gradient (15–90 °C) within an extremely acidic hydrothermal system (Pisciarelli Spring, Campi Flegrei area, southern Italy) displayed how hydrothermal fluids influence the microbial dynamics. This area was characterized by high levels of reduced gaseous species (e.g. H2S, H2, CH4, CO), and very low pH values (<2.3). Thermodynamic calculations revealed a high microbial catabolic potential in oxidation/reduction reactions of N-, S-, and Fe-bearing species. Overall, an increase of the archaeal/bacterial abundance ratio was observed by decreasing temperature and pH values. In particular, Archaea and Bacteria were present in almost equal cell abundance (up to 1.1 × 109 and 9.3 × 108 cell/g, respectively) in the <70 °C sampling points (average pH = 2.09); on the contrary, highest temperature waters (85–90 °C; average pH = 2.26) were characterized by low abundance of archaeal cells. The high-throughput sequencing of 16S rRNA gene indicated strong differences in archaeal and bacterial communities’ composition along temperature gradient. However, the microbiome in this extreme environment was mainly constituted by chemoautotrophic microorganisms that were likely involved in N-, S-, and Fe-bearing species transformations (e.g. Acidianus infernus, Ferroplasma acidarmanus, Acidithiobacillus, Sulfobacillus, Thaumarchaeota), in agreement with thermodynamic calculations.
Cataglyphis are thermophilic ants that forage during the day when temperatures are highest and sometimes close to their critical thermal limit. Several Cataglyphis species have evolved unusual reproductive systems such as facultative queen parthenogenesis or social hybridogenesis, which have not yet been investigated in detail at the molecular level. We generated high-quality genome assemblies for two hybridogenetic lineages of the Iberian ant Cataglyphis hispanica using long-read Nanopore sequencing and exploited chromosome conformation capture (3C) sequencing to assemble contigs into 26 and 27 chromosomes, respectively. Further karyotype analyses confirm this difference in chromosome numbers between lineages; however, they also suggest it may not be fixed among lineages. We obtained transcriptomic data to assist gene annotation and built custom repeat libraries for each of the two assemblies. Comparative analyses with 19 other published ant genomes were also conducted. These new genomic resources pave the way for exploring the genetic mechanisms underlying the remarkable thermal adaptation and the molecular mechanisms associated with transitions between different genetic systems characteristic of the ant genus Cataglyphis.
Diatoms are important contributors to marine primary production and the ocean carbon cycle. In the North Atlantic and its adjacent seas primary production is driven by diatoms that transfer a significant part of the produced energy to higher trophic levels and carbon to the deep ocean. Anthropogenic warming and climate variability will likely have important consequences for the productivity and spatial dynamics of these eukaryotic phytoplankton. Using multidecadal diatom abundance data (>60 years) for the Northeast Atlantic and the North Sea, we show significant spatial and temporal correlations over these scales between diatoms and climate variability. A general multidecadal trend is established where climate warming is increasing diatom populations in northerly systems but decreasing populations in more southerly systems. We discover major phase shifts in diatom abundance synchronous with multi-decadal trends in Atlantic climate variability that occurred after the mid-1990s.
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145 members
Christopher J Frederickson
  • Zinc Signaling Laboratory
Anton F Post
  • Josephine Bay Paul Center for Comparative Molecular Biology and Evolution
Carsten Wolff
  • Department of Research
Fernando Rodriguez
  • Josephine Bay Paul Center for Comparative Molecular Biology and Evolution
Karen Echeverri
  • Bell Center for Regenerative Biology and Tissue Engineering
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