Microbial Surface Colonization and Biofilm Development in Marine Environments

Abstract

Biotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.

FIG 1

Key processes of the marine carbon cycle. Microorganisms colonize the surfaces of most marine organisms, such as phytoplankton, zooplankton, protists, and fish, and marine particles, including phytoplankton detritus, zooplankton and fish fecal pellets, and marine snow. The surface-associated microbiota participate in mutualistic or antagonistic interactions with algae or zooplankton. They also play important roles (indicated by asterisks) in the degradation and remineralization of particulate organic matter and in the enhancement of primary production (via inorganic nutrient regeneration to fuel phytoplankton in the euphotic zone and chemolithoautotrophic microbial communities in the aphotic zone). The surface-associated microbiota also influence long-term carbon sequestration in the ocean via both the biological pump and the microbial carbon pump mechanisms. All the respiration terms are omitted so that the graph is not too cluttered. Abbreviations: POC, particulate organic carbon; DOC, dissolved organic carbon.

FIG 2

Interacting sensing, signaling, and regulatory pathways important for the Vibrio cholerae sessile lifestyle. Diverse environmental cues such as chitin disaccharide and oligosaccharides, bile acids (not shown), nitric oxide, norspermidine (not shown), spermidine, carbon source depletion, and population size signals (such as the autoinducers cholerae autoinducer 1 [CAI-1] and autoinducer 2 [AI-2]) are sensed and processed by V. cholerae, which employs signal transduction sensor kinases (such as ChiS, VarS, LuxQ, CqsS, CqsR, VpsS, and HnoK) and response regulators (such as LuxO, VarA, HnoB, HnoD, TfoX, VpsR, and VpsT); the quorum-sensing master transcriptional regulators AphA and HapR; small RNAs (such as CsrB, CsrC, CsrD, Qrr1 to -4, and TfoR); and the RNA chaperone Hfq, cAMP, and c-di-GMP for signal relay and response regulation. The type IV pili are involved in initial surface attachment. The activated production of VPS (Vibrio polysaccharide) (the major component of the V. cholerae biofilm matrix) and biofilm matrix proteins contributes to biofilm formation. It is evident that most regulatory pathways converge on c-di-GMP, which plays a central role governing the microbial switch from the planktonic to the sessile lifestyle. There are some other surface- and biofilm-related sensing, signaling, and regulatory pathways, such as the CqsR and VpsS QS pathways that are functionally redundant to the CqsA/CqsS and LuxS/LuxPQ QS pathways, the chemotactic pathway that senses extracellular chitin disaccharide and oligosaccharides and modulates bacterial tactic movement toward chitin surfaces for efficient colonization and chitin utilization, the stringent response regulatory pathway that maximizes the use of available resources in response to various low-nutrient stresses, the nucleoside scavenging-and-signaling pathway for regulating natural competence, and the pathways mediated by H-NS and alternative sigma factors, which are not shown in order to avoid cluttering. LCD, low cell population density; HCD, high cell population density; LuxS, autoinducer-2 synthase; LuxP, autoinducer-2 periplasmic binding protein; LuxQ, autoinducer-2 membrane-bound sensor histidine kinase; CqsS, CAI-1 membrane-bound sensor histidine kinase; LuxU, autoinducer phosphorelay protein; LuxO, LuxU cognate response regulator; CBP, chitin-binding protein; NspS, periplasmic spermidine-binding protein; HnoX, NO sensor protein; OM, outer membrane; IM, inner membrane; CsrA, global posttranscriptional regulatory protein that activates LuxO via an unidentified regulatory factor (denoted “?”); Qrr, quorum regulatory small RNA; Hfq, RNA-binding and chaperone protein; cAMP-CRP, cAMP-cAMP receptor protein complex; Fis, factor for inversion stimulation, a small nucleoid protein; PTS, phosphoenolpyruvate phosphotransferase system; CyaA, adenylate cyclase that synthesizes cellular cAMP; VCA0939, CdgA, and the GGDEF domain of MbaA, diguanylate cyclases that synthesize cellular c-di-GMP; HnoB and the EAL domain of MbaA, phosphodiesterases that degrade c-di-GMP; HnoD, protein containing a degenerate phosphodiesterase functioning as an HnoB allosteric inhibitor; VpsR and VpsT, transcriptional regulators that modulate VPS synthesis, with VpsR also being a regulator of V. cholerae biofilm matrix protein synthesis; T2SS, type II secretion system; com, msh, rbm, and vps, gene operons for chitin-induced natural competence, type IV pilus production, biofilm matrix protein production, and VPS production, respectively. This figure is drawn based on information reported previously (15, 49, 51, 338, 414, 420, 470–472, 475, 491, 500, 505, 511, 512, 527).