Diatom adhesive trail proteins acquired by horizontal gene transfer from bacteria serve as primers for marine biofilm formation

Abstract

Biofilm-forming benthic diatoms are key primary producers in coastal habitats, where they frequently dominate sunlit submerged and intertidal substrata. The development of a unique form of gliding motility in raphid diatoms was a key molecular adaptation that contributed to their evolutionary success. Gliding motility is hypothesized to be driven by an intracellular actin-myosin motor and requires the secretion of polysaccharide- and protein-based adhesive materials. To date, the structure-function correlation between diatom adhesives utilized for gliding and their relationship to the extracellular matrix that constitutes the diatom biofilm is unknown. Proteomics analysis of the adhesive material from Craspedostauros australis revealed eight novel, diatom-specific proteins. Four of them constitute a new family of proteins, named Trailins, which contain an enigmatic domain termed Choice-of-Anchor-A (CAA). Immunostaining demonstrated that Trailins are only present in the adhesive trails required to generate traction on native substrata, but are absent from the extracellular matrix of biofilms. Phylogenetic analysis and Protein 3D structure prediction suggests that the CAA-domains in Trailins were obtained from bacteria by horizontal gene transfer, and exhibit a striking structural similarity to ice-binding proteins. Our work advances the understanding of the molecular basis for diatom underwater adhesion and biofilm formation providing evidence that there is a molecular switch between proteins required for initial surface colonization and those required for 3D biofilm matrix formation.

Gliding motility of the diatom Craspedostauros australis correlates with the intracellular movement of raphid-specific myosins

“…As gliding motility is restricted to raphid diatoms, we performed a phylogenomic analysis on all publicly available diatom myosin sequences to determine which myosins are specific to raphid diatoms. BLAST analysis of the C. australis genome assembly 27,28 revealed twelve putative myosin sequences, a number which is similar to other sequenced diatoms ( Phaeodactylum tricornutum : 10; Thalassiosira pseudonana : 11) 34 . The phylogenomic analysis was performed using the motor domains of 320 diatom myosins from 52 diatom species ( Supplementary Fig.…”

“…Some of these EPS strands, in particular those not connected to the AMC, may exert elastic or frictional counterforces potentially causing a dissipation of energy during force transmission 50 . Recent findings have started to unveil the molecular composition of the diatom EPS and identified two exceptionally large modular proteins in the C. australis adhesive trails (CaTrailin4; ~900 kDa and Ca5609; >1 mDa) 28 , which may contribute to these counterforces, and a mucin-like protein (CaFAP1) 27 that may contribute to reducing the frictional resistance between the cell and the substratum. However, how these components, and others, contribute to mediating interactions between the intracellular cytoskeleton, the cell surface and the substratum beneath remain to be investigated.…”

“…To date, no diatom myosin has been functionally characterized. Recent advances in genetic engineering of the raphid diatom Craspedostauros australis [26][27][28] have enabled new approaches to investigate the proposed role of myosins as force generators during diatom gliding. In this study, we aim to test this hypothesis by identifying raphid-specific myosins through phylogenomic analysis and by relating their intracellular dynamic behavior to cell movement.…”

Microbial colonization patterns and biodegradation of petrochemical and biodegradable plastics in lake waters: insights from a field experiment

“…The presence of Rhodobacteriaceae on PET, Cyanobiaceae on LDPE and PLA, along with microalgae and diatoms in all the polymers tested, might provide a further attachment substratum for bacteria. Biofilm-forming cyanobacteria and diatoms are known to highly contribute to EPS secretion ( Duan et al, 2023 ; Raghavan et al, 2023 ; Romeu et al, 2023 ; Zackova Suchanova et al, 2023 ), decreasing the chance for the bacterial populations, including those potentially suitable to degrade polymers, to be in direct contact with plastic surfaces. Moreover, Cyanobacteria and microalgae provide assimilable organic matter (e.g., photosynthates, EPS) ( Underwood and Paterson, 2003 ), that is more likely to be used as growth substrate than carbon of plastic materials.…”

Transcriptional chronology reveals conserved genes involved in pennate diatom sexual reproduction

“…edu/ genom escope) using a maximum k-mer coverage of 1000 (Figure 2d). To detect contigs that are potentially derived from bacterial contamination, each transcript was taxonomically classified with Kraken2 (Wood et al, 2019) using a custom database containing Kraken2 RefSeq protein sequences (archaea, bacteria, human, fungi, plants and protozoa), all PLAZA Diatoms v1.0 proteomes (Osuna-Cruz et al, 2020) and the proteins of the decontaminated MMETSP dataset (Keeling et al, 2014;Van Vlierberghe et al, 2021), whose homology-based translation was described in Zackova Suchanova et al (Zackova Suchanova et al, 2023). Next, we screened for potentially contaminated contigs where all genes were taxonomically annotated as being derived from bacteria, but could detect none among the contigs containing >3 genes.…”