Metaorganisms as the new frontier

Abstract

Summary Because it appears that almost all organisms are part of an interdependent meta-organism, an understanding of the underlying host-microbe species associations, and of its evolution and molecular underpinnings, has become the new frontier in zoology. The availability of novel highthroughput sequencing methods together with the conceptual understanding that advances mostly originate at the intersection of traditional disciplinary boundaries, enable biologists to dissect the mechanisms that control the interdependent associations of species. In this perspective article, we outline some of the issues in interspecies interactions, present two case studies illuminating the necessity of interfacial research when addressing complex and fundamental zoological problems, and show that an interdisciplinary approach that seeks to understand co-evolved multi-species relationships will connect genomes, phenotypes, ecosystems and the evolutionary forces that have shaped them. We hope that this article inspires other collaborations of a similar nature on the diverse landscape commonly referred to as “zoology”.

The many faces of biological individuality

“…The fact that virtually every living thing is home to ''foreign passengers''-some of which play important functional roles in the host-raises important issues regarding biological boundaries, individuality criteria based on genetic homogeneity, etc. (Gilbert 2002;Bosch and McFall-Ngai 2011;Gilbert and Epel 2015). Building on recent philosophical work on symbiosis (Pradeu and Carosella 2006;Bouchard 2009;Dupré and O'Malley 2009;Pradeu 2011;Godfrey-Smith 2013;Booth 2014b;O'Malley 2016), the contributors of this special issue examine symbiosis from different, yet complementary points of view.…”

Microbiome shifts and the inhibition of quorum sensing by Black Band Disease cyanobacteria

“…Coral microbiota have important roles in the health of the holobiont and contribute importantly to nutrient acquisition Bosch and McFall-Ngai, 2011). Displacement of primary commensals with other members of the microbiome or shifts in the abundance of microbiome members have been linked with the appearance of disease signs and polymicrobial diseases (Cardenas et al, 2012;Vezzulli et al, 2013;Roder et al, 2014b).…”

Organisms or biological individuals? Combining physiological and evolutionary individuality

“…But it is important to recognise that a major result of recent biological research is precisely that very often a physiological individual is not as such a reproducing entity, but rather a local nexus of different lineages of reproducing entities. Indeed, work on symbiosis has shown that virtually all physiological individuals are multispecies units (Pradeu and Carosella 2006;Dupré and O'Malley 2009;Bosch and McFall-Ngai 2011;Pradeu 2012), functionallyintegrated wholes that unify an extraordinarily diverse range of living constituents -in particular bacteria (Bäckhed et al 2005;Faith et al 2013), fungi (Underhill andIliev 2014), andviruses (Virgin 2014). Such a physiological whole does not include as its constituents all the microbes that are in or on the host, only those that both interact strongly with other host's constituents and make a critical contribution to the functioning and survival of the whole.…”

“…Organisms as diverse as plants, marine animals such as ascidians and corals, insects or mammals, harbour a tremendous number of microbes that play a key role in their physiological activitiesdigestion, immune defence, development, etc. -at least in natural conditions (Bosch and McFall-Ngai 2011;McFall-Ngai et al 2013;Oldroyd 2013). Germ-free organisms (i.e., organisms raised in the lab, who do not possess normal microbiota) have many physiological defects, and usually cannot live and reproduce normally outside strict laboratory conditions (Xu and Gordon 2003).…”