The seaweed holobiont: Understanding seaweed-bacteria interactions
TL;DR: Recent advances in the understanding of macroalgal-bacterial interactions with reference to the diversity and functional role of epiphytic bacteria in maintaining algal health are reported, highlighting the holobiont concept.
Abstract: Seaweeds (macroalgae) form a diverse and ubiquitous group of photosynthetic organisms that play an essential role in aquatic ecosystems These ecosystem engineers contribute significantly to global primary production and are the major habitat formers on rocky shores in temperate waters, providing food and shelter for aquatic life Like other eukaryotic organisms, macroalgae harbor a rich diversity of associated microorganisms with functions related to host health and defense In particular, epiphytic bacterial communities have been reported as essential for normal morphological development of the algal host, and bacteria with antifouling properties are thought to protect chemically undefended macroalgae from detrimental, secondary colonization by other microscopic and macroscopic epibiota This tight relationship suggests that macroalgae and epiphytic bacteria interact as a unified functional entity or holobiont, analogous to the previously suggested relationship in corals Moreover, given that the impact of diseases in marine ecosystems is apparently increasing, understanding the role of bacteria as saprophytes and pathogens in seaweed communities may have important implications for marine management strategies This review reports on the recent advances in the understanding of macroalgal–bacterial interactions with reference to the diversity and functional role of epiphytic bacteria in maintaining algal health, highlighting the holobiont concept
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TL;DR: Recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed and questions are posed for targeted investigation of surface-specific community-level microbial features to advance understanding ofsurface-associated microbial community ecology and the biogeochemical functions of these communities.
Abstract: SUMMARY Biotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.
696 citations
Cites background from "The seaweed holobiont: Understandin..."
...(252), and prone to leading a surface-associated life (12, 17, 246, 272, 574, 607) supported by the extracellular degradation of complex biopolymers such as polysaccharides and proteins (194, 791, 794–797)....
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TL;DR: The concept of holobionts as dynamic ecosystems that interact at multiple scales and respond to environmental change is discussed and the link between environmental perturbations, dysbiosis, and sponge diseases is discussed.
Abstract: The recognition that all macroorganisms live in symbiotic association with microbial communities has opened up a new field in biology. Animals, plants, and algae are now considered holobionts, complex ecosystems consisting of the host, the microbiota, and the interactions among them. Accordingly, ecological concepts can be applied to understand the host-derived and microbial processes that govern the dynamics of the interactive networks within the holobiont. In marine systems, holobionts are further integrated into larger and more complex communities and ecosystems, a concept referred to as “nested ecosystems.” In this review, we discuss the concept of holobionts as dynamic ecosystems that interact at multiple scales and respond to environmental change. We focus on the symbiosis of sponges with their microbial communities—a symbiosis that has resulted in one of the most diverse and complex holobionts in the marine environment. In recent years, the field of sponge microbiology has remarkably advanced in terms of curated databases, standardized protocols, and information on the functions of the microbiota. Like a Russian doll, these microbial processes are translated into sponge holobiont functions that impact the surrounding ecosystem. For example, the sponge-associated microbial metabolisms, fueled by the high filtering capacity of the sponge host, substantially affect the biogeochemical cycling of key nutrients like carbon, nitrogen, and phosphorous. Since sponge holobionts are increasingly threatened by anthropogenic stressors that jeopardize the stability of the holobiont ecosystem, we discuss the link between environmental perturbations, dysbiosis, and sponge diseases. Experimental studies suggest that the microbial community composition is tightly linked to holobiont health, but whether dysbiosis is a cause or a consequence of holobiont collapse remains unresolved. Moreover, the potential role of the microbiome in mediating the capacity for holobionts to acclimate and adapt to environmental change is unknown. Future studies should aim to identify the mechanisms underlying holobiont dynamics at multiple scales, from the microbiome to the ecosystem, and develop management strategies to preserve the key functions provided by the sponge holobiont in our present and future oceans.
333 citations
Cites background from "The seaweed holobiont: Understandin..."
...Marine microbes exist not only in a planktonic state but also in symbiosis with macroorganisms: animals, plants, and algae alike [3, 4]....
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18 May 2020
TL;DR: Tax4Fun2 is an R package for the prediction of functional profiles and functional gene redundancies of prokaryotic communities from 16S rRNA gene sequences that is easy-to-use, platform-independent and highly memory-efficient, thus enabling researchers without extensive bioinformatics knowledge or access to high-performance clusters to predict functional profiles.
Abstract: Sequencing of 16S rRNA genes has become a powerful technique to study microbial communities and their responses towards changing environmental conditions in various ecosystems. Several tools have been developed for the prediction of functional profiles from 16S rRNA gene sequencing data, because numerous questions in ecosystem ecology require knowledge of community functions in addition to taxonomic composition. However, the accuracy of these tools relies on functional information derived from genomes available in public databases, which are often not representative of the microorganisms present in the studied ecosystem. In addition, there is also a lack of tools to predict functional gene redundancy in microbial communities. To address these challenges, we developed Tax4Fun2, an R package for the prediction of functional profiles and functional gene redundancies of prokaryotic communities from 16S rRNA gene sequences. We demonstrate that functional profiles predicted by Tax4Fun2 are highly correlated to functional profiles derived from metagenomes of the same samples. We further show that Tax4Fun2 has higher accuracies than PICRUSt and Tax4Fun. By incorporating user-defined, habitat-specific genomic information, the accuracy and robustness of predicted functional profiles is substantially enhanced. In addition, functional gene redundancies predicted with Tax4Fun2 are highly correlated to functional gene redundancies determined for simulated microbial communities. Tax4Fun2 provides researchers with a unique tool to predict and investigate functional profiles of prokaryotic communities based on 16S rRNA gene sequencing data. It is easy-to-use, platform-independent and highly memory-efficient, thus enabling researchers without extensive bioinformatics knowledge or access to high-performance clusters to predict functional profiles. Another unique feature of Tax4Fun2 is that it allows researchers to calculate the redundancy of specific functions, which is a potentially important measure of how resilient a community will be to environmental perturbation. Tax4Fun2 is implemented in R and freely available at https://github.com/bwemheu/Tax4Fun2.
246 citations
TL;DR: Epibiotic microorganisms associated with marine algae and invertebrates have a high antifouling (AF) potential, which can be used to solve biofouling problems in industry, however, more information about the production of AF compounds by marine microorganisms in situ and their mechanisms of action needs to be obtained.
Abstract: Any natural or artificial substratum exposed to seawater is quickly fouled by marine microorganisms and later by macrofouling species. Microfouling organisms on the surface of a substratum form heterogenic biofilms, which are composed of multiple species of heterotrophic bacteria, cyanobacteria, diatoms, protozoa and fungi. Biofilms on artificial structures create serious problems for industries worldwide, with effects including an increase in drag force and metal corrosion as well as a reduction in heat transfer efficiency. Additionally, microorganisms produce chemical compounds that may induce or inhibit settlement and growth of other fouling organisms. Since the last review by the first author on inhibition of biofouling by marine microbes in 2006, significant progress has been made in the field. Several antimicrobial, antialgal and antilarval compounds have been isolated from heterotrophic marine bacteria, cyanobacteria and fungi. Some of these compounds have multiple bioactivities. Microorganisms are...
242 citations
Cites background from "The seaweed holobiont: Understandin..."
...…of AF compounds (Qian et al. 2010; Fusetani 2011), larval settlement (Hadfield 2010; Thiyagarajan 2010), properties of epibiotic bacteria (Egan et al. 2008, 2012; Penesyan et al. 2010; Harder et al. 2012; Wahl et al. 2012) and chemical ecology (Paul & Ritson-Williams 2008; Paul et al.…...
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TL;DR: Algae derivatives have shown promise as candidates in novel, antibacterial drug discovery and applications as antibiotics, disinfectants, and inhibitors of foodborne pathogenic and spoilage bacteria are reviewed in this article.
Abstract: The marine environment is home to a taxonomically diverse ecosystem. Organisms such as algae, molluscs, sponges, corals, and tunicates have evolved to survive the high concentrations of infectious and surface-fouling bacteria that are indigenous to ocean waters. Both macroalgae (seaweeds) and microalgae (diatoms) contain pharmacologically active compounds such as phlorotannins, fatty acids, polysaccharides, peptides, and terpenes which combat bacterial invasion. The resistance of pathogenic bacteria to existing antibiotics has become a global epidemic. Marine algae derivatives have shown promise as candidates in novel, antibacterial drug discovery. The efficacy of these compounds, their mechanism of action, applications as antibiotics, disinfectants, and inhibitors of foodborne pathogenic and spoilage bacteria are reviewed in this article.
232 citations
Cites background from "The seaweed holobiont: Understandin..."
...[7], where the presence of the Vibrio actually contributes to successful algal reproduction, allowing the two organisms to function as a holobiont [27]....
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References
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TL;DR: The understanding of the effect of viruses on global systems and processes continues to unfold, overthrowing the idea that viruses and virus-mediated processes are sidebars to global processes.
Abstract: Viruses exist wherever life is found. They are a major cause of mortality, a driver of global geochemical cycles and a reservoir of the greatest genetic diversity on Earth. In the oceans, viruses probably infect all living things, from bacteria to whales. They affect the form of available nutrients and the termination of algal blooms. Viruses can move between marine and terrestrial reservoirs, raising the spectre of emerging pathogens. Our understanding of the effect of viruses on global systems and processes continues to unfold, overthrowing the idea that viruses and virus-mediated processes are sidebars to global processes.
1,894 citations
"The seaweed holobiont: Understandin..." refers background in this paper
...Viruses are abundant in the marine environment and have been extensively studied in the plankton and for their role in ocean nutrient cycling (see (Suttle, 2005) and references there in)....
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Cornell University1, University of Maryland, College Park2, North Carolina State University3, University of Maryland Biotechnology Institute4, Harvard University5, University of Southern Mississippi6, Old Dominion University7, University of South Florida St. Petersburg8, Erasmus University Rotterdam9, University of Georgia10, University of South Carolina Aiken11
TL;DR: A dramatic global increase in the severity of coral bleaching in 1997-98 is coincident with high El Niño temperatures, which climate-mediated, physiological stresses may compromise host resistance and increase frequency of opportunistic diseases.
Abstract: Mass mortalities due to disease outbreaks have recently affected major taxa in the oceans. For closely monitored groups like corals and marine mammals, reports of the frequency of epidemics and the number of new diseases have increased recently. A dramatic global increase in the severity of coral bleaching in 1997—98 is coincident with high El Nino temperatures. Such climate-mediated, physiological stresses may compromise host resistance and increase frequency of opportunistic diseases. Where documented, new diseases typically have emerged through host or range shifts of known pathogens. Both climate and human activities may have also accelerated global transport of species, bringing together pathogens and previously unexposed host populations. T he oceans harbor enormous biodiver- sity by terrestrial terms (1), much of which is still poorly described taxo- nomically. Even less well known are the dy- namics of intermittent, ephemeral, threshold phenomena such as disease outbreaks. De- spite decades of intense study of the biolog- ical agents structuring natural communities, the ecological and evolutionary impact of diseases in the ocean remains unknown, even when these diseases affect economically and ecologically important species. The paucity of baseline and epidemiological information on normal disease levels in the ocean chal- lenges our ability to assess the novelty of a recent spate of disease outbreaks and to de- termine the relative importance of increased pathogen transmission versus decreased host resistance in facilitating the outbreaks. Our objectives here are to review the prevalence of diseases of marine taxa to evaluate wheth- er it can be concluded that there has been a recent increase. We also assess the contribut- ing roles of human activity and global cli- mate, and evaluate the role of the oceans as incubators and conveyors of human disease agents. Is There an Increase in Diseases in the Ocean?
1,778 citations
"The seaweed holobiont: Understandin..." refers background in this paper
...…interest in microbial disease in marine ecosystems is, in part, driven by concerns that climate change-related stress on marine habitat formers (corals, macroalgae, etc.) and their associated microbiome will render them more susceptible to potential opportunistic pathogens (Harvell et al., 1999)....
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TL;DR: The ecology of sponge-microbe associations is examined, including the establishment and maintenance of these sometimes intimate partnerships, the varied nature of the interactions (ranging from mutualism to host-pathogen relationships), and the broad-scale patterns of symbiont distribution.
Abstract: Marine sponges often contain diverse and abundant microbial communities, including bacteria, archaea, microalgae, and fungi. In some cases, these microbial associates comprise as much as 40% of the sponge volume and can contribute significantly to host metabolism (e.g., via photosynthesis or nitrogen fixation). We review in detail the diversity of microbes associated with sponges, including extensive 16S rRNA-based phylogenetic analyses which support the previously suggested existence of a sponge-specific microbiota. These analyses provide a suitable vantage point from which to consider the potential evolutionary and ecological ramifications of these widespread, sponge-specific microorganisms. Subsequently, we examine the ecology of sponge-microbe associations, including the establishment and maintenance of these sometimes intimate partnerships, the varied nature of the interactions (ranging from mutualism to host-pathogen relationships), and the broad-scale patterns of symbiont distribution. The ecological and evolutionary importance of sponge-microbe associations is mirrored by their enormous biotechnological potential: marine sponges are among the animal kingdom's most prolific producers of bioactive metabolites, and in at least some cases, the compounds are of microbial rather than sponge origin. We review the status of this important field, outlining the various approaches (e.g., cultivation, cell separation, and metagenomics) which have been employed to access the chemical wealth of sponge-microbe associations.
1,262 citations
"The seaweed holobiont: Understandin..." refers background in this paper
...Mesophilic Crenarchaeota have been observed in many marine habitats, including sessile invertebrates such as sponges, where they are thought to play a key role in the oxidation of ammonia (Taylor et al., 2007; Turque et al., 2010)....
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TL;DR: Generalization of the coral probiotic hypothesis has led to the hologenome theory of evolution, which proposes the occurrence of a dynamic relationship between symbiotic microorganisms and corals that selects for the coral holobiont that is best suited for the prevailing environmental conditions.
Abstract: Coral microbiology is an emerging field, driven largely by a desire to understand, and ultimately prevent, the worldwide destruction of coral reefs. The mucus layer, skeleton and tissues of healthy corals all contain large populations of eukaryotic algae, bacteria and archaea. These microorganisms confer benefits to their host by various mechanisms, including photosynthesis, nitrogen fixation, the provision of nutrients and infection prevention. Conversely, in conditions of environmental stress, certain microorganisms cause coral bleaching and other diseases. Recent research indicates that corals can develop resistance to specific pathogens and adapt to higher environmental temperatures. To explain these findings the coral probiotic hypothesis proposes the occurrence of a dynamic relationship between symbiotic microorganisms and corals that selects for the coral holobiont that is best suited for the prevailing environmental conditions. Generalization of the coral probiotic hypothesis has led us to propose the hologenome theory of evolution.
1,261 citations
"The seaweed holobiont: Understandin..." refers background in this paper
...2), in line with what has been suggested for the coral holobiont (Rosenberg et al., 2007; Bourne et al., 2009)....
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TL;DR: The diversity of chemosynthetic symbionts and their hosts is focused on, and phylogenetic analyses have shown that these associations have evolved on multiple occasions by convergent evolution.
Abstract: Chemosynthetic symbioses occur in a wide range of ocean habitats, from deep-sea vents and cold seeps to whale falls and shallow-water sediments. This Review reveals the diversity and complexity of these symbioses, some of which include multiple symbiotic partners. Chemosynthetic symbioses between bacteria and marine invertebrates were discovered 30 years ago at hydrothermal vents on the Galapagos Rift. Remarkably, it took the discovery of these symbioses in the deep sea for scientists to realize that chemosynthetic symbioses occur worldwide in a wide range of habitats, including cold seeps, whale and wood falls, shallow-water coastal sediments and continental margins. The evolutionary success of these symbioses is evident from the wide range of animal groups that have established associations with chemosynthetic bacteria; at least seven animal phyla are known to host these symbionts. The diversity of the bacterial symbionts is equally high, and phylogenetic analyses have shown that these associations have evolved on multiple occasions by convergent evolution. This Review focuses on the diversity of chemosynthetic symbionts and their hosts, and examines the traits that have resulted in their evolutionary success.
852 citations
"The seaweed holobiont: Understandin..." refers background in this paper
...…clear that many marine eukaryotes possess stable associations with bacterial partners and depend on them for growth, development, supply of nutrients as well as protection from colonization and predation (Dubilier et al., 2008; Egan et al., 2008; Crawford & Clardy, 2011; Wahl et al., 2012)....
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...It is becoming clear that many marine eukaryotes possess stable associations with bacterial partners and depend on them for growth, development, supply of nutrients as well as protection from colonization and predation (Dubilier et al., 2008; Egan et al., 2008; Crawford & Clardy, 2011; Wahl et al., 2012)....
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