scholarly journals A community perspective on the concept of marine holobionts: current status, challenges, and future directions

Author(s):  
Simon M Dittami ◽  
Enrique Arboleda ◽  
Jean-Christophe Auguet ◽  
Arite Bigalke ◽  
Enora Briand ◽  
...  

Host-microbe interactions play crucial roles in marine ecosystems, but we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a stable relationship, form the holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences with comparisons to terrestrial sciences where appropriate. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g. the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. The most significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This will be crucial to decipher the roles of marine holobionts in biogeochemical cycles, but also developing concrete applications of the holobiont concept e.g. to increase yield or disease resistance in aquacultures or to protect and restore marine ecosystems through management projects.

Author(s):  
Simon M Dittami ◽  
Enrique Arboleda ◽  
Jean-Christophe Auguet ◽  
Arite Bigalke ◽  
Enora Briand ◽  
...  

Host-microbe interactions play crucial roles in marine ecosystems, but we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a stable relationship, form the holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences with comparisons to terrestrial sciences where appropriate. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g. the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. The most significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This will be crucial to decipher the roles of marine holobionts in biogeochemical cycles, but also developing concrete applications of the holobiont concept e.g. to increase yield or disease resistance in aquacultures or to protect and restore marine ecosystems through management projects.


2019 ◽  
Author(s):  
Simon M Dittami ◽  
Enrique Arboleda ◽  
Jean-Christophe Auguet ◽  
Arite Bigalke ◽  
Enora Briand ◽  
...  

Host-microbe interactions play crucial roles in marine ecosystems, but we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a stable relationship, form the holobiont, and have to be studied together, as a coherent biological and functional unit, to understand its biology, ecology and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences with comparisons to terrestrial science wherever appropriate. Given the connectivity and the unexplored biodiversity of marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances. For the marine scientific community, the most significant challenge is to bridge functional research on tractable and original model systems and global approaches addressing ecological and evolutionary questions. This will be crucial for establishing the roles of marine holobionts in biogeochemical cycles, but also developing concrete applications of the holobiont concept in aquaculture and marine ecosystem management projects.


PeerJ ◽  
2021 ◽  
Vol 9 ◽  
pp. e10911
Author(s):  
Simon M. Dittami ◽  
Enrique Arboleda ◽  
Jean-Christophe Auguet ◽  
Arite Bigalke ◽  
Enora Briand ◽  
...  

Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g., the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever.


Author(s):  
Simon M Dittami ◽  
Enrique Arboleda ◽  
Jean-Christophe Auguet ◽  
Arite Bigalke ◽  
Enora Briand ◽  
...  

Host-microbe interactions play crucial roles in marine ecosystems, but we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a long-lasting relationship, form the holobiont, and have to be studied together, as a coherent biological and functional unit, in order to understand the biology, ecology and evolution of the organisms. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences with comparisons to terrestrial science whenever appropriate. A deeper understanding of such complex systems, however, will require further technological and conceptual advances. The most significant challenge will be to bridge functional research on simple and tractable model systems and global approaches. This will require scientists to work together as an (inter)active community in order to address, for instance, ecological and evolutionary questions and the roles of holobionts in biogeochemical cycles.


1995 ◽  
Vol 73 (12) ◽  
pp. 1675-1685 ◽  
Author(s):  
Thomas E. Massey ◽  
Randall G. Leeder ◽  
Elizabeth Rafeiro ◽  
James F. Brien

Although amiodarone is a highly efficacious antidysrhythmic agent, the drug produces numerous adverse effects. The most critical of these is pulmonary toxicity because of the potential for mortality. This review examines the experimental model systems used to study amiodarone toxicity, summarizes the current state of knowledge regarding the processes involved in amiodarone-induced pulmonary toxicity (AIPT), and includes a discussion of potential future directions. Possible contributing processes to initiation of AIPT include phospholipidosis, altered calcium ion regulation, generation of reactive oxygen species, formation of an amiodarone aryl radical, and perturbation of cellular energy production. In addition, an immune response to the parent compound or to a metabolite could play a role. It is expected that elucidation of the mechanism(s) of AIPT will lead to safer antidysrhythmic agents and (or) to effective treatments for the prevention or amelioration of AIPT.Key words: amiodarone, pulmonary fibrosis, oxidative stress, pulmonary toxicity, pneumonitis.


2021 ◽  
Vol 3 (1) ◽  
Author(s):  
Ting-bei Bo ◽  
Kevin D. Kohl

AbstractMany animals engage in a behavior known as natal philopatry, where after sexual maturity they return to their own birthplaces for subsequent reproduction. There are many proposed ultimate factors that may underlie the evolution of natal philopatry, such as genetic optimization, suitable living conditions, and friendly neighbors, which can improve the survival rates of offspring. However, here we propose that a key factor that has been overlooked could be the colonization of gut microbiota during early life and the effects these microorganisms have on host performance and fitness. In addition to the bacteria transmitted from the mother to offspring, microbes from the surrounding environment also account for a large proportion of the developing gut microbiome. While it was long believed that microbial species all have global distributions, we now know that there are substantial geographic differences and dispersal limitations to environmental microbes. The establishment of gut microbiota during early life has enormous impacts on animal development, including energy metabolism, training of the immune system, and cognitive development. Moreover, these microbial effects scale to influence animal performance and fitness, raising the possibility for natural selection to act on the integrated combination of gut microbial communities and host genetics (i.e. the holobiont). Therefore, in this paper, we propose a hypothesis: that optimization of host-microbe-environment interactions represents a potentially important yet overlooked reason for natal philopatry. Microbiota obtained by natal philopatry could help animals adapt to the environment and improve the survival rates of their young. We propose future directions to test these ideas, and the implications that this hypothesis has for our understanding of host-microbe interactions.


mSphere ◽  
2020 ◽  
Vol 5 (1) ◽  
Author(s):  
Charlotte De Rudder ◽  
Marta Calatayud Arroyo ◽  
Sarah Lebeer ◽  
Tom Van de Wiele

ABSTRACT The epithelium of the human sinonasal cavities is colonized by a diverse microbial community, modulating epithelial development and immune priming and playing a role in respiratory disease. Here, we present a novel in vitro approach enabling a 3-day coculture of differentiated Calu-3 respiratory epithelial cells with a donor-derived bacterial community, a commensal species (Lactobacillus sakei), or a pathobiont (Staphylococcus aureus). We also assessed how the incorporation of macrophage-like cells could have a steering effect on both epithelial cells and the microbial community. Inoculation of donor-derived microbiota in our experimental setup did not pose cytotoxic stress on the epithelial cell layers, as demonstrated by unaltered cytokine and lactate dehydrogenase release compared to a sterile control. Epithelial integrity of the differentiated Calu-3 cells was maintained as well, with no differences in transepithelial electrical resistance observed between coculture with donor-derived microbiota and a sterile control. Transition of nasal microbiota from in vivo to in vitro conditions maintained phylogenetic richness, and yet a decrease in phylogenetic and phenotypic diversity was noted. Additional inclusion and coculture of THP-1-derived macrophages did not alter phylogenetic diversity, and yet donor-independent shifts toward higher Moraxella and Mycoplasma abundance were observed, while phenotypic diversity was also increased. Our results demonstrate that coculture of differentiated airway epithelial cells with a healthy donor-derived nasal community is a viable strategy to mimic host-microbe interactions in the human upper respiratory tract. Importantly, including an immune component allowed us to study host-microbe interactions in the upper respiratory tract more in depth. IMPORTANCE Despite the relevance of the resident microbiota in sinonasal health and disease and the need for cross talk between immune and epithelial cells in the upper respiratory tract, these parameters have not been combined in a single in vitro model system. We have developed a coculture system of differentiated respiratory epithelium and natural nasal microbiota and incorporated an immune component. As indicated by absence of cytotoxicity and stable cytokine profiles and epithelial integrity, nasal microbiota from human origin appeared to be well tolerated by host cells, while microbial community composition remained representative for that of the human (sino)nasal cavity. Importantly, the introduction of macrophage-like cells enabled us to obtain a differential readout from the epithelial cells dependent on the donor microbial background to which the cells were exposed. We conclude that both model systems offer the means to investigate host-microbe interactions in the upper respiratory tract in a more representative way.


2019 ◽  
Author(s):  
TY Fofanova ◽  
CJ Stewart ◽  
JM Auchtung ◽  
RL Wilson ◽  
RA Britton ◽  
...  

AbstractMechanistic investigations of host-microbe interactions in the human gut are limited by current co-culture model systems. The intestinal epithelium requires oxygen for viability, while gut bacteria are facultative or obligate anaerobes. The ability to model host-commensal interactions under dynamic oxygen conditions is critical to understanding host-pathogen interactions in the human gut. Here, we demonstrate a simple, cost-effective method for co-culturing obligate anaerobic bacteria with human intestinal enteroid monolayers under variable oxygen conditions. The Enteroid-Anaerobe Co-Culture (EACC) system is able to recapitulate the steep oxygen gradient seenin vivoand induce expression of hypoxia-associated phenotypes such as increased barrier integrity and expression of antimicrobial peptide genes. Using clinical strains of the commensal anaerobesBacteroides thetaiotaomicronandBlautiasp. on established patient-derived intestinal enteroid cell lines under physiological hypoxia, the EACC system can sustain host-anaerobe interactions for at least 24 hours. Following co-culture with anaerobic bacteria, we demonstrate patient-specific differences in epithelial response, reinforcing the potential to develop a personalized medicine approach to bacteriotherapy and host-microbe interaction investigations. Our innovative EACC system provides a robust model for investigating host-microbe interactions in complex, patient-derived intestinal tissues, that facilitates study of mechanisms underlying the role of the microbiome in health and disease.


2017 ◽  
Vol 312 (6) ◽  
pp. G623-G627 ◽  
Author(s):  
Vincent B. Young

There has been an explosion of interest in studying the indigenous microbiota, which plays an important role in human health and disease. Traditionally, the study of microbes in relationship to human health involved consideration of individual microbial species that caused classical infectious diseases. With the interest in the human microbiome, an appreciation of the influence that complex communities of microbes can have on their environment has developed. When considering either individual pathogenic microbes or a symbiotic microbial community, researchers have employed a variety of model systems with which they can study the host-microbe interaction. With the use of studies of infections with the toxin-producing bacterium Clostridium difficile as a model for both a pathogen and beneficial bacterial communities as an example, this review will summarize and compare various model systems that can be used to gain insight into the host-microbe interaction.


2011 ◽  
Vol 208 (11) ◽  
pp. 2159-2162 ◽  
Author(s):  
Daniel D. Rockey

Chlamydial plasmids are small, highly conserved, nonconjugative, and nonintegrative DNA molecules that are nearly ubiquitous in many chlamydial species, including Chlamydia trachomatis. There has been significant recent progress in understanding chlamydial plasmid participation in host–microbe interactions, disease, and immune responses. Work in mouse model systems and, very recently, in nonhuman primates demonstrates that plasmid-deficient chlamydial strains function as live attenuated vaccines against genital and ocular infections. Collectively, these studies open new avenues of research into developing vaccines against trachoma and sexually transmitted chlamydial infections.


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