Metaorganisms as the new frontier

Abstract

Because it appears that almost all organisms are part of an interdependent metaorganism, an understanding of the underlying host-microbe species associations, and of evolution and molecular underpinnings, has become the new frontier in zoology. The availability of novel high-throughput 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 review article, we outline some of the issues in inter-species 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".

Figure 1. Karl August Möbius and the biocenosis concept

(A) Karl August Möbius, Gemälde von Ernst Hildebrand, 1895. (B) Möbius´ study object: the molluscs in the North Sea. From: H. A. Meyer, K. Möbius: Fauna der Kieler Bucht. Erster Band: Die Hinterkiemer oder Opisthobranchia. Zweiter Band: Die Prosobranchia und Lamellibranchia nebst einem Supplement zu den Ophistobranchia. Engelmann. Leipzig 1865–1872

Figure 2

Multicellular organisms are metaorganism comprised of the macroscopic host and synergistic interdependence with bacteria, archaea, fungi, and numerous other microbial and eukaryotic species including algal symbionts.

Figure 3. Selected model organisms allow integrated analysis of host-symbiont interactions

(A) Termites live in symbiosis with cellulose-degrading gut microbes (© Bayer). (B) Hydra is a new model organism for epithelial host-microbe interactions. (C) Pathogenic effects of a disturbed host-microbe homeostasis have been discovered in mice (© ONRL). (D) Aphids harbor the symbiont Buchnera aphidicola, which supplies the host with essential amino acids, that are not included in the phloem sap diet (© Alex Wild). (E) The bacterium Vibrio fisherii induces the formation of the light organ in the squid E. scolopes (picture taken from M. J. McFall-Ngai and E. G. Ruby). (F) The coral bleaching disease is a global threat of coral reefs. Changes in the microbiota of the coral host can confer resistance to bleaching (© Lee James Pantas). (G) The gut development of the zebrafish Danio rerio is dependent on the presence of gut bacteria.