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

Covariation patterns of Phytoplankton and Bacterioplankton in hypertrophic shallow lakes

The aim of this work was to assess the temporal patterns in the community composition of phytoplankton (PCC) and bacterioplankton (BCC) in two interconnected and hypertrophic Pampean shallow lakes in Argentina. Factors shaping their community dynamics and community temporal covariations were also analysed. We performed 4 years of seasonal samplings (2012-2016) and communities were studied by the Utermöhl approach (PCC) and Illumina MiSeq sequencing (BCC). We found marked seasonal variations in both communities and inter-annual variations with decreasing microbial community similarities during the study. We also observed covariation in community-level dynamics among PCC and BCC within and between shallow lakes. The within-lake covariations remained positive and significant, while controlling for the effects of intrinsic (environmental) and extrinsic (temporal and meteorological) factors, suggesting a community coupling mediated by intrinsic biotic interactions. Algal-bacterial associations between different taxa of phytoplankton and bacterioplankton within each lake were also found. PCC was mainly explained by pure regional extrinsic (17-21%) and intrinsic environmental (8-9%) factors, while BCC was explained by environmental (8-10%) and biotic interactions with phytoplankton (7-8%). Our results reveal that the influence of extrinsic regional factors can be channeled to bacterioplankton through both environmental (i.e. water temperature) and phytoplankton effects.Fil: Schiaffino, María Romina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires. Universidad Nacional del Noroeste de la Provincia de Buenos Aires. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires; ArgentinaFil: Huber, Maria Paula. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto Nacional de Limnología. Universidad Nacional del Litoral. Instituto Nacional de Limnología; ArgentinaFil: Sagua, Mara Inés. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires. Universidad Nacional del Noroeste de la Provincia de Buenos Aires. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires; ArgentinaFil: Sabio y García, Carmen Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Reissig, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; Argentin

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

Phylogenetic Diversity, Host-Specificity and Community Profiling of Sponge-Associated Bacteria in the Northern Gulf of Mexico

Marine sponges can associate with abundant and diverse consortia of microbial symbionts. However, associated bacteria remain unexamined for the majority of host sponges and few studies use phylogenetic metrics to quantify symbiont community diversity. DNA fingerprinting techniques, such as terminal restriction fragment length polymorphisms (T-RFLP), might provide rapid profiling of these communities, but have not been explicitly compared to traditional methods.We investigated the bacterial communities associated with the marine sponges Hymeniacidon heliophila and Haliclona tubifera, a sympatric tunicate, Didemnum sp., and ambient seawater from the northern Gulf of Mexico by combining replicated clone libraries with T-RFLP analyses of 16S rRNA gene sequences. Clone libraries revealed that bacterial communities associated with the two sponges exhibited lower species richness and lower species diversity than seawater and tunicate assemblages, with differences in species composition among all four source groups. T-RFLP profiles clustered microbial communities by source; individual T-RFs were matched to the majority (80.6%) of clone library sequences, indicating that T-RFLP analysis can be used to rapidly profile these communities. Phylogenetic metrics of community diversity indicated that the two sponge-associated bacterial communities include dominant and host-specific bacterial lineages that are distinct from bacteria recovered from seawater, tunicates, and unrelated sponge hosts. In addition, a large proportion of the symbionts associated with H. heliophila were shared with distant, conspecific host populations in the southwestern Atlantic (Brazil).The low diversity and species-specific nature of bacterial communities associated with H. heliophila and H. tubifera represent a distinctly different pattern from other, reportedly universal, sponge-associated bacterial communities. Our replicated sampling strategy, which included samples that reflect the ambient environment, allowed us to differentiate resident symbionts from potentially transient or prey bacteria. Pairing replicated clone library construction with rapid community profiling via T-RFLP analyses will greatly facilitate future studies of sponge-microbe symbioses

Longitudinal survey of microbiome associated with particulate matter in a megacity.

BackgroundWhile the physical and chemical properties of airborne particulate matter (PM) have been extensively studied, their associated microbiome remains largely unexplored. Here, we performed a longitudinal metagenomic survey of 106 samples of airborne PM2.5 and PM10 in Beijing over a period of 6 months in 2012 and 2013, including those from several historically severe smog events.ResultsWe observed that the microbiome composition and functional potential were conserved between PM2.5 and PM10, although considerable temporal variations existed. Among the airborne microorganisms, Propionibacterium acnes, Escherichia coli, Acinetobacter lwoffii, Lactobacillus amylovorus, and Lactobacillus reuteri dominated, along with several viral species. We further identified an extensive repertoire of genes involved in antibiotic resistance and detoxification, including transporters, transpeptidases, and thioredoxins. Sample stratification based on Air Quality Index (AQI) demonstrated that many microbial species, including those associated with human, dog, and mouse feces, exhibit AQI-dependent incidence dynamics. The phylogenetic and functional diversity of air microbiome is comparable to those of soil and water environments, as its composition likely derives from a wide variety of sources.ConclusionsAirborne particulate matter accommodates rich and dynamic microbial communities, including a range of microbial elements that are associated with potential health consequences

Bacterial community profiles and Vibrio parahaemolyticus abundance in individual oysters and their association with estuarine ecology

Oysters naturally harbor the human gastric pathogen Vibrio parahaemolyticus, but the nature of this association is unknown. Because microbial interactions could influence the accumulation of V. parahaemolyticus in oysters, we investigated the composition of the microbiome in water and oysters at two ecologically unique sites in the Great Bay Estuary, New Hampshire using 16s rRNA profiling. We then evaluated correlations between bacteria inhabiting the oyster with V. parahaemolyticus abundance quantified using a most probable number (MPN) analysis. Even though oysters filter-feed, their microbiomes were not a direct snapshot of the bacterial community in overlaying water, suggesting they selectively accumulate some bacterial phyla. The microbiome of individual oysters harvested more centrally in the bay were relatively more similar to each other and had fewer unique phylotypes, but overall more taxonomic and metabolic diversity, than the microbiomes from tributary-harvested oysters that were individually more variable with lower taxonomic and metabolic diversity. Oysters harvested from the same location varied in V. parahaemolyticus abundance, with the highest abundance oysters collected from one location. This study, which to our knowledge is the first of its kind to evaluate associations of V. parahaemolyticus abundance with members of individual oyster microbiomes, implies that sufficient sampling and depth of sequencing may reveal microbiome members that could impact V. parahaemolyticus abundance

Extended local similarity analysis (eLSA) of microbial community and other time series data with replicates

© The Author(s), 2011. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Systems Biology 5 Suppl 2 (2011): S15, doi:10.1186/1752-0509-5-S2-S15.The increasing availability of time series microbial community data from metagenomics and other molecular biological studies has enabled the analysis of large-scale microbial co-occurrence and association networks. Among the many analytical techniques available, the Local Similarity Analysis (LSA) method is unique in that it captures local and potentially time-delayed co-occurrence and association patterns in time series data that cannot otherwise be identified by ordinary correlation analysis. However LSA, as originally developed, does not consider time series data with replicates, which hinders the full exploitation of available information. With replicates, it is possible to understand the variability of local similarity (LS) score and to obtain its confidence interval. We extended our LSA technique to time series data with replicates and termed it extended LSA, or eLSA. Simulations showed the capability of eLSA to capture subinterval and time-delayed associations. We implemented the eLSA technique into an easy-to-use analytic software package. The software pipeline integrates data normalization, statistical correlation calculation, statistical significance evaluation, and association network construction steps. We applied the eLSA technique to microbial community and gene expression datasets, where unique time-dependent associations were identified. The extended LSA analysis technique was demonstrated to reveal statistically significant local and potentially time-delayed association patterns in replicated time series data beyond that of ordinary correlation analysis. These statistically significant associations can provide insights to the real dynamics of biological systems. The newly designed eLSA software efficiently streamlines the analysis and is freely available from the eLSA homepage, which can be accessed at http://meta.usc.edu/softs/lsaThis research is partially supported by the National Science Foundation (NSF) DMS-1043075 and OCE 1136818

Sustaining rare marine microorganisms: macroorganisms as repositories and dispersal agents of microbial diversity

Recent analyses revealed that most of the biodiversity observed in marine microbial communities is represented by organisms with low abundance but, nonetheless essential for ecosystem dynamics and processes across both temporal and spatial scales. Surprisingly, few studies have considered the effect of macroorganism-microbe interactions on the ecology and distribution dynamics of rare microbial taxa. In this review, we synthesize several lines of evidence that these relationships cannot be neglected any longer. First, we provide empirical support that the microbiota of macroorganisms represents a significant part of marine bacterial biodiversity and that host-microbe interactions benefit to certain microbial populations which are part of the rare biosphere (i.e., opportunistic copiotrophic organisms). Second, we reveal the major role that macroorganisms may have on the dispersal and the geographic distribution of microbes. Third, we introduce an innovative and integrated view of the interactions between microbes and macroorganisms, namely sustaining the rares, which suggests that macroorganisms favor the maintenance of marine microbial diversity and are involved in the regulation of its richness and dynamics. Finally, we show how this hypothesis complements existing theories in microbial ecology and offers new perspectives about the importance of macroorganisms for the microbial biosphere, particularly the rare members

Microbiologia molecular na aquacultura: em busca de uma comunidade microbiana saudável

The microbial communities of aquaculture systems are involved in maintaining the health and growth of farmed organisms. They participate in nutrient cycling, nutrition, disease control and water quality of the system and effluents. We use DGGE fingerprint techniques and high-throughput sequencing analyzes to access the semi-intensive and intensive aquaculture microbiota. First, we investigated the composition of the bacterioplankton communities of a recirculating aquaculture system (RAS) used for the production of juveniles sole (Solea senegalensis). The most abundant orders detected in the aquaculture of sole were: Alteromonadales, Rhodobacterales, Oceanospirillales, Vibrionales and Flavobacteriales. OTUs related to potential fish pathogens in aquaculture systems were detected, as well as naturally occurring probiotic bacteria. These may have played a role in suppressing potential pathogens of fish, keeping the aquaculture free from disease. In an aquaculture of adult sole, the presence of fish was described as the main factor influencing bacterial composition. Here, supply water served as an important seed bank for the colonization of bacterial populations in the hatchery RAS tanks, mainly related to probiotic bacteria. The importance of this compartment for the maintenance of a healthy aquaculture and its importance in the development of strategies for microbial manipulation/management of aquaculture was reinforced. Subsequently, we describe the seasonal dynamics and potential interactions of bacterial and microeukaryotic plankton communities in a semi-intensive aquaculture for European sea bass (Dicentrarchus labrax) over a year. The most abundant bacterial classes were Gammaproteobacteria, Flavobacteriia and Alphaproteobacteria; while the microeukaryotic communities were dominated by the Ochrophyta, Chlorophyta and Ciliophora groups. Here, in addition to the potential effects of abiotic parameters on microbial plankton, there was a correlation between bacterial and microeukaryote populations which may be an indication of trophic and / or metabolic interdependence between these two domains. These studies allowed us to describe the normal microbiota of aquaculture systems, their ecological interactions and the impacts exerted by environmental factors in order to support the development of strategies for the maintenance of a productive and healthy environment.As comunidades microbianas dos sistemas de aquacultura estão envolvidas na manutenção da saúde e crescimento dos organismos cultivados. Participam no ciclo dos nutrientes, nutrição, controle de doenças e qualidade da água do sistema e efluentes. Neste trabalho foram utilizadas técnicas independentes de cultivo (Denaturing Gradient Gel Electrophoresis e sequenciação) para caracterizar o microbioma da água de um sistema semi-intensivo e um sistema intensivo de aquacultura de peixes. Primeiro, investigamos a composição das comunidades bacterioplânctonicas de um sistema de aquacultura recirculante (SRA) utilizado para a produção de juvenis de linguado (Solea senegalensis). As ordens mais abundantes detectadas nas aquaculturas de liguado foram: Alteromonadales, Rhodobacterales, Oceanospirillales, Vibrionales e Flavobacteriales. Foram detetadas sequências com similaridade a espécies potencialmente patogénicas, assim como sequências com similaridade a grupos previamente descritos como probióticos. É discutido o papel destas ultimas na supressão dos potenciais patógenos de peixes e manutenção de um ambiente saudável (sem surtos de doenças). Numa aquacultura de adultos de linguados, a presença dos peixes foi descrita como um dos principais fatores determinantes na composição das comunidades bacterianas. Aqui, a água atuou como um importante banco de sementes para a colonização de populações bacterianas nos tanques do SRA, principalmente das relacionadas às bactérias probióticas. Este trabalho demonstra que a origem da água pode ter um papel relevante na manutenção de uma comunidade microbiana saudável, reforçando a sua importância em possíveis estratégias de manipulação/gestão microbiana das aquaculturas. Posteriormente, descrevemos a dinâmica sazonal e potenciais interações das comunidades de plâncton bacteriano e microeucariótico em uma aquicultura semi-intensiva para robalo (Dicentrarchus labrax) durante um ano. As classes bacterianas mais abundantes foram Gammaproteobacteria, Flavobacteriia e Alphaproteobacteria; enquanto a comunidades microeucariotica foi dominada pelos grupos Ochrophyta, Chlorophyta e Ciliophora. Aqui, além dos efeitos potenciais dos parâmetros abióticos no plâncton microbiano, houve correlação entre as populações de bactérias e microeucariotos o que pode ser uma indicação de interdependência trófica e / ou metabólica entre estes dois domínios. Estes estudos permitiram-nos descrever o microbioma normal de sistemas de aquacultura, suas interações ecológicas e os impactos exercidos pelos fatores ambientais com o intuito de fundamentar o desenvolvimento de estratégias para a manutenção de um ambiente produtivo e saudável.Programa Doutoral em Biologi

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