A complex journey: transmission of microbial symbionts

Abstract

The perpetuation of symbioses through host generations relies on symbiont transmission. Horizontally transmitted symbionts are taken up from the environment anew by each host generation, and vertically transmitted symbionts are most often transferred through the female germ line. Mixed modes also exist. In this Review we describe the journey of symbionts from the initial contact to their final residence. We provide an overview of the molecular mechanisms that mediate symbiont attraction and accumulation, interpartner recognition and selection, as well as symbiont confrontation with the host immune system. We also discuss how the two main transmission modes shape the evolution of the symbiotic partners.Symbiont transmission maintains symbioses through host generations and has a pivotal role in their evolution 1 -5 . Despite growing evidence that microbial associations are present in diverse animals and plants in virtually every environment, our knowledge of the mechanisms of symbiont transmission is restricted to a few model systems. Most of these involve bacteria and some archaea 6 , 7 (Supplementary information S1 (table)). Two fundamentally different modes of transmission can be distinguished: horizontal (that is, from an environmental, free-living symbiont source) and vertical (that is, inheritance of the symbiont from the mother or, more rarely, from both parents). However, there is great variation, and transmission can also be mixed, involving both vertical and horizontal transfers from the environment and intraspecific or interspecific host switching (FIG. 1).This Review focuses on those associations that maintain protracted physical contact and involve most of the host population. We use de Bary's definition of symbiosis: living together of differently named organisms 8 , irrespective of the effects of the interaction on the fitness of the partners 9 . The key question is how the symbiont is transferred to the host progeny, regardless of the type of symbiosis. Reviews are already available for a range of symbiotic systems: plants 10 -16 , sponges 17 , 18 , chemosynthetic bacteria-marine invertebrates 19 , 20 , entomopathogenic nematodes 21 , 22 , annelids 23 , 24 , insects 25 -30 , squid 31 , 32 © 2010 Macmillan Publishers Limited. All rights reserved monika.bright@univie.ac.at; silvia.bulgheresi@univie.ac.at. Competing interests statementThe authors declare no competing financial interests. 33 -36 . Here, we review how the conversation between partners, which ultimately integrates the symbiont into the host's life cycle, is initiated. By identifying the similarities and differences between the two principal types of symbiont transmission, we explore their evolutionary implications. DATABASES Horizontal transmissionThe cyclic occurrence of aposymbiotic (that is, before the symbiont is acquired) and symbiotic phases in the host's life cycle is intrinsic to horizontally transmitted symbionts (Boxes 1,2; FIG. 2) (Supplementary information S1 (table)). In animal hosts, the aposymbiotic phase inc...

Endofungal bacterium controls its host by an hrp type III secretion system

“…Furthermore, phylogenetic studies of a number of rhizoxinpositive isolates from all the five continents, delivered evidence for host switching of symbionts between fungal lineages (Lackner et al, 2009a), indicating that horizontal transmission has taken place during evolution of the symbiosis, and might still have a role in the natural environment. Yet, in each reproduction cycle of the fungus, B. rhizoxinica is passed on vertically to the next generation, which is a hallmark of close mutualistic relationships (Moran, 2006;Bright and Bulgheresi, 2010). Quite unexpectedly, we observed that the host is not capable of vegetative reproduction in the absence of endosymbionts.…”

“…In particular, the transmission of the endosymbionts during host reproduction is a critical step for their survival. Impressive studies document the manifold strategies to ensure a permanent association of bacteria with partners of the animal and plant kingdoms (Dale and Moran, 2006;Moran, 2006;Bright and Bulgheresi, 2010). In stark contrast, nothing is known about the molecular basis of the transmission of endofungal bacteria, that is, bacteria that reside within the fungal cytosol (Kobayashi and Crouch, 2009;Tarkka et al, 2009).…”

Epidemic Spread of Symbiotic and Non-Symbiotic Bradyrhizobium Genotypes Across California

“…Of particular interest are host-associated bacteria, including pathogens and symbionts. These diverse bacterial lineages colonize host surfaces, inhabit specific tissues or cells, and can often persist free in soils and or aquatic habitats between phases of host infection [1,2]. The capacity of bacteria to thrive in host tissues is often modulated by the presence of plasmids and genomic islands, cassettes of accessory loci that can get transmitted among genomes.…”

Organisms or biological individuals? Combining physiological and evolutionary individuality

“…For example, it is commonly said that, on the long run, evolution will favour the internalization of symbiotic microbes into the host and their vertical transmission, but what we observe in practice is different: in many cases, such as the ancient and stable legume-rhizobia association, we observe complex intimate interactions, reoccurring in an horizontal way at each generation (Bright and Bulgheresi 2010) (Kiers et al 2003;Oldroyd 2013), instead of vertical transmission.…”

“…In some cases, for instance in arthropods, many members of the microbiota are transmitted vertically (from parents to offspring). In other cases, for instance in mammals and in many plants, a majority of the members of the microbiota are transmitted horizontally (i.e., they are acquired from the environment) (Bright and Bulgheresi 2010) 19 . In the case of vertical transmission, physiological individuals understood as host-microbe associations can be highly-realised Darwinian individuals, because lineages of these associations can be established.…”