The epiphytic microbiota of the globally widespread macroalga Cladophora glomerata (Chlorophyta, Cladophorales)

Abstract

• Premise of the study: The filamentous chlorophyte Cladophora produces abundant nearshore populations in marine and freshwaters worldwide, often dominating periphyton communities and producing nuisance growths under eutrophic conditions. High surface area and environmental persistence foster such high functional and taxonomic diversity of epiphytic microfauna and microalgae that Cladophora has been labeled an ecological engineer. We tested the hypotheses that (1) Cladophora supports a structurally and functionally diverse epiphytic prokaryotic microbiota that influences materials cycling and (2) mutualistic host–microbe interactions occur. Because previous molecular sequencing‐based analyses of the microbiota of C. glomerata found as western Lake Michigan beach drift had identified pathogenic associates such as Escherichia coli, we also asked if actively growing lentic C. glomerata harbors known pathogens. • Methods: We used 16S rRNA gene amplicon pyrosequencing to examine the microbiota of C. glomerata of Lake Mendota, Dane, Wisconsin, United States, during the growing season of 2011, at the genus‐ or species‐level to infer functional phenotypes. We used correlative scanning electron and fluorescence microscopy to describe major prokaryotic morphotypes. • Key results: We found microscopic evidence for diverse bacterial morphotypes, and molecular evidence for ca. 100 distinct sequence types classifiable to genus at the 80% confidence level or species at the 96–97% level within nine bacterial phyla, but not E. coli or related human pathogens. • Conclusions: We inferred that bacterial epiphytes of lentic C. glomerata have diverse functions in materials cycling, with traits that indicate the occurrence of mutualistic interactions with the algal host.

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

“…Widespread algal-methanotroph associations should be expected to occur because, like peat mosses and other wetland plants (Fausser et al 2012), photosynthetic algae provide a reliable supply of oxygen needed for methanotrophy and an extensive area of stable attachment surface in methane-rich habitats. The results we report here and elsewhere (Zulkifly et al 2012;Graham et al 2014a) suggest that, as in the case of peat moss-methanotroph associations, algal-associated methanotrophy may help to control the accumulation of methane in Earth's atmosphere today and also has done so in the remote past. The metagenomic indications of algal-associated methanotrophy observed in this study justify future functional studies of methane dynamics in modern algal communities that might allow models of ancient methanotrophy to be constructed from fossil evidence.…”

“…The community of identifiable bacterial genera for periphytic Cladophora sampled at the same time and from a geographically close freshwater system analyzed in the same way (Graham et al 2015) was considerably less similar to those of the streptophytes we examined than were streptophyte microbiota compared to each other. Evidence for Rhizobium, common to most of the streptophyte microbiotas reported here, was absent from both amplicon (Zulkifly et al 2012) and metagenomic sequences of the chlorophyte Cladophora (Graham et al 2015).…”

“…The absence of Rhizobium from the microbiota of the outgroup chlorophyte Cladophora sampled from similar environments and time periods and examined by both amplicon analysis (Zulkifly et al 2012) and metagenomics (Graham et al 2015) further supports the concept that streptophytes may have forged specific and persistent associations with rhizobialeans early in the history of the plant lineage. Our observations suggest that (1) streptophyterhizobialean associations may be much older than previously thought, likely predating the colonization of land; (2) land plants likely inherited from ancestral algae the ability to form beneficial associations with N-fixing bacteria; and (3) ancient streptophyes, like modern descendants, had multiple sources of microbe-fixed nitrogen that provided resilience to environmental variation and change.…”

“…Our metagenomic evidence that methanotrophs occur in the microbiotas of aquatic streptophyte algae in addition to those of nonstreptophyte periphytic freshwater algae (Zulkifly et al 2012;Graham et al 2014a) is important because freshwaters are known hot spots of methane production (Bastviken et al 2011). Widespread algal-methanotroph associations should be expected to occur because, like peat mosses and other wetland plants (Fausser et al 2012), photosynthetic algae provide a reliable supply of oxygen needed for methanotrophy and an extensive area of stable attachment surface in methane-rich habitats.…”

“…Bacterial epibionts are known to occur widely among algae, likely providing essential vitamins such as B 12 (cobalamin) and performing other ecological functions hypothesized to foster algal survival (Fisher and Wilcox 1996;Fisher et al 1998;Croft et al 2005;Zulkifly et al 2012Zulkifly et al , 2013Graham et al 2014aGraham et al , 2014b. Because land plants inherited key structural and reproductive traits from ancestral green algae , it seems likely that algal ancestors might similarly have bequeathed the ability to form beneficial microbial associations to land plant descendants.…”