Microbiomes of Streptophyte Algae and Bryophytes Suggest That a Functional Suite of Microbiota Fostered Plant Colonization of Land

Abstract

Premise of research. The origin of land plants catalyzed key changes in Earth's atmosphere and biota. Microbial associations likely nurtured earliest plants and influenced their biogeochemical roles. Because angiosperm and animal microbiomes-bacteria, archaea, microbial eukaryotes, and genes that promote host survival-are known to display lineage effects, we hypothesized that microbiomes of early-diverging modern bryophytes and phylogenetically closely related green algae might likewise reveal commonalities reflecting ancestral traits.Methodology. New metagenomic sequence data were obtained for the late-diverging streptophyte algae Chaetosphaeridium globosum and Coleochaete pulvinata and the liverwort Conocephalum conicum, representing early-diverging land plants. New 16S rDNA amplicon sequences were acquired for the charalean Nitella tenuissima. Sequence data were used to infer bacterial genera and fungi for comparisons among streptophyte microbiota and with our published microbiome data for the outgroup chlorophyte Cladophora. To enhance evolutionary signal, taxa were sampled in the same time frame and from geographically close locales. Streptophyte metagenomic data were also probed for protein markers of significant physiological and biogeochemical functions: NifH indicating nitrogen fixation, particulate MMo indicating methane oxidation, and vitamin B 12 (cobalamin) indicating biosynthetic pathway enzymes.Pivotal results. Microbiota of studied streptophytes consistently included diverse N-fixing cyanobacteria and/or Rhizobiales, as well as methanotrophs and early-diverging fungi, and were more similar to each other than to Cladophora microbiota. Streptophyte metagenomic data indicated diverse nifH (nitrogen fixation) and pMMo (methane oxidation) marker sequences and vitamin B 12 pathway genes. Glomalean fungi occurred with Conocephalum, consistent with field studies of modern liverworts and microfossil evidence for cooccurrence of glomaleans and early land plants. Conclusions.A suite of N fixers, methanotrophs, cobalamin producers, and early-diverging fungi was consistently associated with modern streptophyte algae and bryophytes studied, suggesting features of early land plants that have played significant, previously unrecognized roles in global nitrogen and carbon cycling for hundreds of millions of years.

On plant defense signaling networks and early land plant evolution

“…Knack and colleagues [37] performed a metagenomic study of aquatic streptophyte alga- and liverwort-associated microbes, including epiphytic microorganisms (e.g. those growing in the mucilage of streptophyte algae) as well as those colonizing the tissue.…”

“…those growing in the mucilage of streptophyte algae) as well as those colonizing the tissue. Their analyses of three higher-branching streptophyte algae ( Coleochaete pulvinate, Chaetosphaeridium globosum and Nitella tenuissima ) identified potentially beneficial microbes, for example nitrogen-fixing or cobalamin-producing bacteria, but also potentially harmful ones, such as bacteria associated with cellulose degradation [37]. Interestingly, Knack and colleagues [37] also detected some fungi in metagenomic data, an observation that warrants further investigation.…”

“…Their analyses of three higher-branching streptophyte algae ( Coleochaete pulvinate, Chaetosphaeridium globosum and Nitella tenuissima ) identified potentially beneficial microbes, for example nitrogen-fixing or cobalamin-producing bacteria, but also potentially harmful ones, such as bacteria associated with cellulose degradation [37]. Interestingly, Knack and colleagues [37] also detected some fungi in metagenomic data, an observation that warrants further investigation. Among the streptophyte algae investigated, the detected signals included sequences stemming from fungi belonging to the Cryptomycota and Chytridiomycota [37].…”

“…Interestingly, Knack and colleagues [37] also detected some fungi in metagenomic data, an observation that warrants further investigation. Among the streptophyte algae investigated, the detected signals included sequences stemming from fungi belonging to the Cryptomycota and Chytridiomycota [37]. For the investigated liverwort Conocephalum conicum an association with glomalean fungi was demonstrated [37].…”

“…Among the streptophyte algae investigated, the detected signals included sequences stemming from fungi belonging to the Cryptomycota and Chytridiomycota [37]. For the investigated liverwort Conocephalum conicum an association with glomalean fungi was demonstrated [37]. …”