Long-term patterns of an interconnected core marine microbiota

Ocean microbes constitute ~ 70% of the marine biomass, are responsible for ~ 50% of the Earth’s primary production and are crucial for global biogeochemical cycles. Marine microbiotas include core taxa that are usually key for ecosystem function. Despite their importance, core marine microbes are relatively unknown, which reflects the lack of consensus on how to identify them. So far, most core microbiotas have been defined based on species occurrence and abundance. Yet, species interactions are also important to identify core microbes, as communities include interacting species. Here, we investigate interconnected bacteria and small protists of the core pelagic microbiota populating a long-term marine-coastal observatory in the Mediterranean Sea over a decade.Versión del edito

Disentangling environmental effects in microbial association networks

Background Ecological interactions among microorganisms are fundamental for ecosystem function, yet they are mostly unknown or poorly understood. High-throughput-omics can indicate microbial interactions through associations across time and space, which can be represented as association networks. Associations could result from either ecological interactions between microorganisms, or from environmental selection, where the association is environmentally driven. Therefore, before downstream analysis and interpretation, we need to distinguish the nature of the association, particularly if it is due to environmental selection or not. Results We present EnDED (environmentally driven edge detection), an implementation of four approaches as well as their combination to predict which links between microorganisms in an association network are environmentally driven. The four approaches are sign pattern, overlap, interaction information, and data processing inequality. We tested EnDED on networks from simulated data of 50 microorganisms. The networks contained on average 50 nodes and 1087 edges, of which 60 were true interactions but 1026 false associations (i.e., environmentally driven or due to chance). Applying each method individually, we detected a moderate to high number of environmentally driven edges—87% sign pattern and overlap, 67% interaction information, and 44% data processing inequality. Combining these methods in an intersection approach resulted in retaining more interactions, both true and false (32% of environmentally driven associations). After validation with the simulated datasets, we applied EnDED on a marine microbial network inferred from 10 years of monthly observations of microbial-plankton abundance. The intersection combination predicted that 8.3% of the associations were environmentally driven, while individual methods predicted 24.8% (data processing inequality), 25.7% (interaction information), and up to 84.6% (sign pattern as well as overlap). The fraction of environmentally driven edges among negative microbial associations in the real network increased rapidly with the number of environmental factors. Conclusions To reach accurate hypotheses about ecological interactions, it is important to determine, quantify, and remove environmentally driven associations in marine microbial association networks. For that, EnDED offers up to four individual methods as well as their combination. However, especially for the intersection combination, we suggest using EnDED with other strategies to reduce the number of false associations and consequently the number of potential interaction hypotheses. Video abstrac

Genetic variation and temperature affects hybrid barriers during interspecific hybridization.

Genomic imprinting regulates parent-specific transcript dosage during seed development and is mainly confined to the endosperm. Elucidation of the function of many imprinted genes has been hampered by the lack of corresponding mutant phenotypes, and the role of imprinting is mainly associated with genome dosage regulation or allocation of resources. Disruption of imprinted genes has also been suggested to mediate endosperm-based post-zygotic hybrid barriers depending on genetic variation and gene dosage. Here, we have analyzed the conservation of a clade from the MADS-box type I class transcription factors in the closely related species Arabidopsis arenosa, A. lyrata, and A. thaliana, and show that AGL36-like genes are imprinted and maternally expressed in seeds of Arabidopsis species and in hybrid seeds between outbreeding species. In hybridizations between outbreeding and inbreeding species the paternally silenced allele of the AGL36-like gene is reactivated in the hybrid, demonstrating that also maternally expressed imprinted genes are perturbed during hybridization and that such effects on imprinted genes are specific to the species combination. Furthermore, we also demonstrate a quantitative effect of genetic diversity and temperature on the strength of the post-zygotic hybridization barrier. Markedly, a small decrease in temperature during seed development increases the survival of hybrid F1 seeds, suggesting that abiotic and genetic parameters play important roles in post-zygotic species barriers, pointing at evolutionary scenarios favoring such effects. OPEN RESEARCH BADGES: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA562212. All sequences generated in this study have been deposited in the National Center for Biotechnology Information Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra/) with project number PRJNA562212

Long-term patterns of an interconnected core marine microbiota

Background Ocean microbes constitute ~ 70% of the marine biomass, are responsible for ~ 50% of the Earth’s primary production and are crucial for global biogeochemical cycles. Marine microbiotas include core taxa that are usually key for ecosystem function. Despite their importance, core marine microbes are relatively unknown, which reflects the lack of consensus on how to identify them. So far, most core microbiotas have been defined based on species occurrence and abundance. Yet, species interactions are also important to identify core microbes, as communities include interacting species. Here, we investigate interconnected bacteria and small protists of the core pelagic microbiota populating a long-term marine-coastal observatory in the Mediterranean Sea over a decade. Results Core microbes were defined as those present in \u3e 30% of the monthly samples over 10 years, with the strongest associations. The core microbiota included 259 Operational Taxonomic Units (OTUs) including 182 bacteria, 77 protists, and 1411 strong and mostly positive (~ 95%) associations. Core bacteria tended to be associated with other bacteria, while core protists tended to be associated with bacteria. The richness and abundance of core OTUs varied annually, decreasing in stratified warmers waters and increasing in colder mixed waters. Most core OTUs had a preference for one season, mostly winter, which featured subnetworks with the highest connectivity. Groups of highly associated taxa tended to include protists and bacteria with predominance in the same season, particularly winter. A group of 13 highly-connected hub-OTUs, with potentially important ecological roles dominated in winter and spring. Similarly, 18 connector OTUs with a low degree but high centrality were mostly associated with summer or autumn and may represent transitions between seasonal communities. Conclusions We found a relatively small and dynamic interconnected core microbiota in a model temperate marine-coastal site, with potential interactions being more deterministic in winter than in other seasons. These core microbes would be essential for the functioning of this ecosystem over the year. Other non-core taxa may also carry out important functions but would be redundant and non-essential. Our work contributes to the understanding of the dynamics and potential interactions of core microbes possibly sustaining ocean ecosystem function

Long-term patterns of an interconnected core marine microbiota

Background Ocean microbes constitute ∼70% of the marine biomass, are responsible for ∼50% of the Earth’s primary production, and are crucial for global biogeochemical cycles. Marine microbiotas include core taxa that are usually key for ecosystem function. Despite their importance, core marine microbes are relatively unknown, which reflects the lack of consensus on how to identify them. So far, most core microbiotas have been defined based on species occurrence and abundance. Yet, species interactions are also important to identify core microbes, as communities include interacting species. Here, we investigate interconnected bacteria and small protists of the core pelagic microbiota populating a long-term marine-coastal observatory in the Mediterranean Sea over a decade. Results Core microbes were defined as those present in >30% of the monthly samples over 10 years, with the strongest associations. The core microbiota included 259 Operational Taxonomic Units (OTUs) including 182 bacteria, 77 protists, and 1,411 strong and mostly positive (∼95%) associations. Core bacteria tended to be associated with other bacteria, while core protists tended to be associated with bacteria. The richness and abundance of core OTUs varied annually, decreasing in stratified warmers waters and increasing in colder mixed waters. Most core OTUs had a preference for one season, mostly winter, which featured subnetworks with the highest connectivity. Groups of highly associated taxa tended to include protists and bacteria with predominance in the same season, particularly winter. A group of 13 highly-connected hub-OTUs, with potentially important ecological roles dominated in winter and spring. Similarly, 18 connector OTUs with a low degree but high centrality were mostly associated with summer or autumn and may represent transitions between seasonal communities. Conclusions We found a relatively small and dynamic interconnected core microbiota in a model temperate marine-coastal site, with potential interactions being more deterministic in winter than in other seasons. These core microbes would be essential for the functioning of this ecosystem over the year. Other non-core taxa may also carry out important functions but would be redundant and non-essential. Our work contributes to the understanding of the dynamics and potential interactions of core microbes possibly sustaining ocean ecosystem function.Preprin

Hybridization of Atlantic puffins in the Arctic coincides with 20th-century climate change

The Arctic is experiencingthe fastest rates of globalwarming,leadingto shiftsin the distributionof its biotaandincreasingthe potentialfor hybridization. However, genomicevidenceof recenthybridization events in theArctic remainsunexpectedlyrare. Here, we use whole-genomesequencingof contemporary and 122-year-oldhistoricalspecimensto investigate the originof an Arctic hybridpopulation of Atlanticpuffins(Fr aterculaarctica)on Bjørnøya, Norway. We show that the hybridization between the High Arctic, large-bodiedsubspeciesF. a. naumanniand the temperate, smaller-sizedsubspeciesF. a. arcticabeganas recentlyas six generationsagodue to an unexpectedsouthward rangeexpansionofF. a. naumanni.Moreover, we find a significanttemporalloss of geneticdiversityacross Arctic and temperate puffinpopulations.Our observationsprovide compellinggenomicevidenceof the impacts of recentdistributionalshiftsand loss of diversityin Arctic communitiesduringthe 20th century.publishedVersio

Microzooplankton distribution in the Amundsen Sea Polynya (Antarctica) during an extensive Phaeocystis antarctica bloom

10 pages, 7 figures, 1 table, supplementary material https://doi.org/10.1016/j.pocean.2018.10.008In Antarctica, summer is a time of extreme environmental shifts resulting in large coastal phytoplankton blooms fueling the food web. Despite the importance of the microbial loop in remineralizing biomass from primary production, studies of how microzooplankton communities respond to such blooms in the Southern Ocean are rather scarce. Microzooplankton (ciliate and dinoflagellate) communities were investigated combining microscopy and 18S rRNA sequencing analyses in the Amundsen Sea Polynya during an extensive summer bloom of Phaeocystis antarctica. The succession of microzooplankton was further assessed during a 15-day induced bloom microcosm experiment. Dinoflagellates accounted for up to 59 % of the microzooplankton biomass in situ with Gymnodinium spp., Protoperidium spp. and Gyrodinium spp. constituting 89 % of the dinoflagellate biomass. Strobilidium spp., Strombidium spp. and tintinids represented 90 % of the ciliate biomass. Gymnodinium, Gyrodinium and tintinnids are known grazers of Phaeocystis, suggesting that this prymnesiophyte selected for the key microzooplankton taxa. Availability of other potential prey, such as diatoms, heterotrophic nanoflagellates and bacteria, also correlated to changes in microzooplankton community structure. Overall, both heterotrophy and mixotrophy appeared to be key trophic strategies of the dominant microzooplankton observed, suggesting that they influence carbon flow in the microbial food web through top-down control on the phytoplankton communityThis work was supported by the Swedish Research Council [grant 2008-6430] to S. Bertilsson and L. Riemann and [grant 824-2008-6429] to P.-O. Moksnes and J. Havenhand, and by the US National Science Foundation through the ASPIRE project [NSF OPP-0839069] to P. YagerPeer Reviewe

Novel interactions between phytoplankton and bacteria shape microbial seasonal dynamics in coastal ocean waters

Trophic interactions between marine phytoplankton and heterotrophic bacteria are at the base of the biogeochemical carbon cycling in the ocean. However, the specific interactions taking place between phytoplankton and bacterial taxa remain largely unexplored, particularly out of phytoplankton blooming events. Here, we applied network analysis to a 3.5-year time-series dataset to assess the specific associations between different phytoplankton and bacterial taxa along the seasonal scale, distinguishing between free-living and particle-attached bacteria. Using a newly developed network post-analysis technique we removed bacteria-phytoplankton correlations that were primarily driven by environmental parameters, to detect potential biotic interactions. Our results indicate that phytoplankton dynamics may be a strong driver of the inter-annual variability in bacterial community composition. We found the highest abundance of specific bacteria-phytoplankton associations in the particle-attached fraction, indicating a tighter bacteria-phytoplankton association than in the free-living fraction. In the particle-associated fraction we unveiled novel potential associations such as the one between Planctomycetes taxa and the diatom Leptocylindrus spp. Consistent correlations were also found between free-living bacterial taxa and different diatoms, including novel associations such as those between SAR11 with Naviculales diatom order, and between Actinobacteria and Cylindrotheca spp. We also confirmed previously known associations between Rhodobacteraceae and Thalassiosira spp. Our results expand our view on bacteria-phytoplankton associations, suggesting that taxa-specific interactions may largely impact the seasonal dynamics of heterotrophic bacterial communities

Disentangling the mechanisms shaping the surface ocean microbiota

BACKGROUND: The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have large-scale consequences. Yet, the underlying ecological mechanisms structuring it are unclear. Here, we investigate how fundamental ecological mechanisms (selection, dispersal and ecological drift) shape the smallest members of the tropical and subtropical surface-ocean microbiota: prokaryotes and minute eukaryotes (picoeukaryotes). Furthermore, we investigate the agents exerting abiotic selection on this assemblage as well as the spatial patterns emerging from the action of ecological mechanisms. To explore this, we analysed the composition of surface-ocean prokaryotic and picoeukaryotic communities using DNA-sequence data (16S- and 18S-rRNA genes) collected during the circumglobal expeditions Malaspina-2010 and TARA-Oceans. RESULTS: We found that the two main components of the tropical and subtropical surface-ocean microbiota, prokaryotes and picoeukaryotes, appear to be structured by different ecological mechanisms. Picoeukaryotic communities were predominantly structured by dispersal-limitation, while prokaryotic counterparts appeared to be shaped by the combined action of dispersal-limitation, selection and drift. Temperature-driven selection appeared as a major factor, out of a few selected factors, influencing species co-occurrence networks in prokaryotes but not in picoeukaryotes, indicating that association patterns may contribute to understand ocean microbiota structure and response to selection. Other measured abiotic variables seemed to have limited selective effects on community structure in the tropical and subtropical ocean. Picoeukaryotes displayed a higher spatial differentiation between communities and a higher distance decay when compared to prokaryotes, consistent with a scenario of higher dispersal limitation in the former after considering environmental heterogeneity. Lastly, random dynamics or drift seemed to have a more important role in structuring prokaryotic communities than picoeukaryotic counterparts. CONCLUSIONS: The differential action of ecological mechanisms seems to cause contrasting biogeography, in the tropical and subtropical ocean, among the smallest surface plankton, prokaryotes and picoeukaryotes. This suggests that the idiosyncrasy of the main constituents of the ocean microbiota should be considered in order to understand its current and future configuration, which is especially relevant in a context of global change, where the reaction of surface ocean plankton to temperature increase is still unclear. Video Abstract

Exploring the oceanic microeukaryotic interactome with metaomics approaches

Contribution to AME Special 6: 'SAME 14: progress and perspectives in aquatic microbial ecology'.-- 12 pages, 4 figures, 4 boxesBiological communities are systems composed of many interacting parts (species, populations or single cells) that in combination constitute the functional basis of the biosphere. Animal and plant ecologists have advanced substantially our understanding of ecological interactions. In contrast, our knowledge of ecological interaction in microbes is still rudimentary. This represents a major knowledge gap, as microbes are key players in almost all ecosystems, particularly in the oceans. Several studies still pool together widely different marine microbes into broad functional categories (e.g. grazers) and therefore overlook fine-grained species/population-specific interactions. Increasing our understanding of ecological interactions is particularly needed for oceanic microeukaryotes, which include a large diversity of poorly understood symbiotic relationships that range from mutualistic to parasitic. The reason for the current state of affairs is that determining ecological interactions between microbes has proven to be highly challenging. However, recent technological developments in genomics and transcriptomics (metaomics for short), coupled with microfluidics and high-performance computing are making it increasingly feasible to determine ecological interactions at the microscale. Here, we present our views on how this field will advance thanks to the progress in metaomics approaches as well as potential avenues for future researchThis work has been supported by the Research Council of Norway (project 240904)Peer Reviewe