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Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom.

ABSTRACT: Diatoms are unicellular algae with a fundamental role in global biogeochemical cycles as major primary producers at the base of aquatic food webs. In recent years, chemical communication between diatoms and associated bacteria has emerged as a key factor in diatom ecology, spurred by conceptual and technological advancements to study the mechanisms underlying these interactions. Here, we use a combination of physiological, transcriptomic, and metabolomic approaches to study the influence of naturally co-existing bacteria, Maribacter sp. and Roseovarius sp., on the sexual reproduction of the biofilm inhabiting marine pennate diatom Seminavis robusta. While Maribacter sp. severely reduces the reproductive success of S. robusta cultures, Roseovarius sp. slightly enhances it. Contrary to our expectation, we demonstrate that the effect of the bacterial exudates is not caused by altered cell-cycle regulation prior to the switch to meiosis. Instead, Maribacter sp. exudates cause a reduced production of diproline, the sexual attraction pheromone of S. robusta. Transcriptomic analyses show that this is likely an indirect consequence of altered intracellular metabolic fluxes in the diatom, especially those related to amino acid biosynthesis, oxidative stress response, and biosynthesis of defense molecules. This study provides the first insights into the influence of bacteria on diatom sexual reproduction and adds a new dimension to the complexity of a still understudied phenomenon in natural diatom populations.

SUBMITTER: Cirri E

PROVIDER: S-EPMC6688387 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Phylogenetic relationships among mediophycean diatoms with elliptical valve outline and elevated apices have long been a subject of interest and debate, particularly with respect to their relationship to pennates. However, results remain inconclusive, whether based on vegetative valve morphology, reproduction, or molecular phylogenetic data. Searching for phylogenetically informative features, we re-examined sexual reproduction, auxospore structure and development in the diatom Biddulphia biddulphiana. Several unique or unusual features and processes characterized its sexual reproduction. A unique spermatogenesis occurs with premeiotic separation of an anucleate protoplast containing all chloroplasts and likely other organelles. Additionally, their auxospore walls are some of the most complex documented, retaining earlier deposited layers that obscure layers formed during later stages of development. The oldest layer consists of thick, mostly organic incunabulum, underlain by outer and inner epizonia and finally transverse (TP) and longitudinal (LP) perizonia. The complexity of the fine structure of these layers is unprecedented. The orientation of some TP bands is also unique in mediophytes, with some perpendicular to the auxospore apical axis, parallel to each other, and open with aligned ends, as typically seen in pennates. The TP also contains rings slanting toward the apices, as in some other mediophytes, e.g., eupodiscaceans. However, both eupodiscaceans and biddulphiaceans show perizonial band structure derived from anastomosing radial scales, thus termed "scaly bands". Pinnate TP bands, common among pennate auxospores, were not found. Thus B. biddulphiana auxospore wall structure contains a mixture of characters specific to this clone but also known from mediophytes and araphid pennates. However, these features do not provide unequivocal evidence that this or the other Biddulphia species examined to date are the closest extant relatives of basal araphid pennates.

Project description:Auxospore production is a sexual reproductive strategy by diatoms to re-attain normal size after the size-reducing effect of clonal reproduction. Aside from the minimum size threshold used as a sex clock by diatoms, the environmental or chemical triggers that can induce sex in diatoms are still not well understood. Here we investigated the influence of six marine bacteria from five families on the production of sexual cells and auxospores of the ubiquitous marine polar centric diatom, Odontella sp. Microbiome association and co-occurrence with the diatom in culture and in nature were investigated using 16S rRNA amplicon sequencing. Indole acetic acid (IAA) secretion, a phytohormone that regulates plants' growth and sexual development, was explored as a potential inducer of sexual reproduction in Odontella and compared between bacterial associates. We found that Odontella co-cultured with Flavobacteriaceae (Polaribacter and Cellulophaga) have significantly more sexual cells and auxospores than bacteria-free Odontella and Odontella co-cultured with other bacteria from Vibrionaceae (Vibrio), Pseudoalteromonadaceae (Pseudoalteromonas), Rhodobacteraceae (Sulfitobacter), or Planococcaceae (Planococcus) family. Differences in IAA secretion were observed between bacterial isolates, but this did not correspond consistently with the diatom's clonal growth or production of sexual cells and auxospores. Microbiome composition survey of Odontella cultures showed that the diatom harbors homologous sequences of the four bacterial isolates at varying proportions, with Sulfitobacter and Polaribacter at high abundances. Microbiome surveys at Santa Cruz Wharf, Monterey Bay, from 2014-2015 showed that Odontella abundance is positively correlated with Flavobacteriaceae and Rhodobacteraceae abundances. Our study demonstrates that specific members of the diatom microbiome can enhance the host's sexual reproduction, with the interkingdom interaction driven by partner compatibility and long-term association. Sex-enhancing bacteria may even be needed by the diatom host to carry out the optimal inducement of sex under normal conditions, allowing for size restitution and maintaining genetic diversity in culture and in nature.

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Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom.

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