Plant-Associated Methylobacteria as Co-Evolved Phytosymbionts

Abstract

Due to their wall-associated pectin metabolism, growing plant cells emit significant amounts of the one-carbon alcohol methanol. Pink-pigmented microbes of the genus Methylobacterium that colonize the surfaces of leaves (epiphytes) are capable of growth on this volatile C1-compound as sole source of carbon and energy. In this article the results of experiments with germ-free (gnotobiotic) sporophytes of angiosperms (sunflower, maize) and gametophytes of bryophytes (a moss and two liverwort species) are summarized. The data show that methylobacteria do not stimulate the growth of these angiosperms, but organ development in moss protonemata and in thalli of liverworts is considerably enhanced. Since methylobacteria produce and secrete cytokinins and auxin, a model of plant-microbe-interaction (symbiosis) is proposed in which the methanol-consuming bacteria are viewed as coevolved partners of the gametophyte that determine its growth, survival and reproduction (fitness). This symbiosis is restricted to the haploid cells of moisture-dependent "living fossil" plants; it does not apply to the diploid sporophytes of higher embryophytes, which are fully adapted to life on land and apparently produce sufficient amounts of endogenous phytohormones.

Methylobacteria isolated from bryophytes and the 2-fold description of the same microbial species

“…2). As detailed elsewhere, 4,7,8 and corroborated by Tani et al, 3 M. funariae is a bryophyte-associated prokaryotic microbe that may also inhabit gametophytes of other cryptogamic plants, such as ferns. Based on our studies and those of others 13 it has been concluded that methylobacteria are methanol-consuming phytosymbionts.…”

“…14 These data, which were generated on greenhousegrown tomato (Lycopersicon esculentum) plants, are difficult to reconcile with the facts that (a) stomata are open during the light period, but closed in the dark, and (b) leaf-associated methylobacteria preferentially occur close to stomatal pores. 8 We conclude that more detailed work on the methylobacterium-gametophyteinteractions are necessary to further explore the postulated "phytosymbionthypothesis" outlined in two articles published in this journal. 4,8 the authors as PPFMs (see ref.…”

“…8 We conclude that more detailed work on the methylobacterium-gametophyteinteractions are necessary to further explore the postulated "phytosymbionthypothesis" outlined in two articles published in this journal. 4,8 the authors as PPFMs (see ref. 6), stimulated organ growth and reproductive development, compared with sterile controls.…”

“…12 Numerous subsequent studies revealed that methylobacteria and bryophytes have, in the course of evolution, established a symbiotic relationship. [6][7][8] In their detailed study, Tani et al 3 document that bacterial strains that belong to the taxa M. adhaesivum, M. brachiatum, M. extorquens, M. marchantiae, M. komagatae and M. radiotolerans, and novel lineages close to M. adhaesivum, most of which were isolated from various bryophytes, are efficient colonizers of the phyllosphere. Based on these data, they speculate that microbes of the genus Methylobacterium preferentially colonize the above groundphytosphere of these "living fossil plants."…”

“…6 Two additional articles on Methylobacterium sp F3.2 followed in 2006 and 2007. 7,8 We also noticed that the information concerning carbohydrate metabolism are erroneous. In Supplemental Table S1, the authors 5 state that "M. bullatum" is not able to metabolize the monosaccharide D-fucose, but in Table S2 a "positive utilization of D-fucose" is highlighted.…”