gels Review From Nano-Gels to Marine Snow: A Synthesis of Gel Formation Processes and Modeling Efforts Involved with Particle Flux in the Ocean Antonietta Quigg 1,* , Peter H. Santschi 2 , Adrian Burd 3, Wei-Chun Chin 4 , Manoj Kamalanathan 1, Chen Xu 2 and Kai Ziervogel 5 1 Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX 77553, USA; [email protected] 2 Department of Marine and Coastal Environmental Science, Texas A&M University at Galveston, Galveston, TX 77553, USA; [email protected] (P.H.S.); [email protected] (C.X.) 3 Department of Marine Science, University of Georgia, Athens, GA 30602, USA; [email protected] 4 Department of Bioengineering, University of California, Merced, CA 95343, USA; [email protected] 5 Institute for the Study of Earth, Oceans and Space, University of New Hampshire, Durham, NH 03824, USA; [email protected] * Correspondence: [email protected] Abstract: Marine gels (nano-, micro-, macro-) and marine snow play important roles in regulating global and basin-scale ocean biogeochemical cycling. Exopolymeric substances (EPS) including transparent exopolymer particles (TEP) that form from nano-gel precursors are abundant materials in the ocean, accounting for an estimated 700 Gt of carbon in seawater. This supports local microbial communities that play a critical role in the cycling of carbon and other macro- and micro-elements in Citation: Quigg, A.; Santschi, P.H.; the ocean. Recent studies have furthered our understanding of the formation and properties of these Burd, A.; Chin, W.-C.; Kamalanathan, materials, but the relationship between the microbial polymers released into the ocean and marine M.; Xu, C.; Ziervogel, K. From snow remains unclear. Recent studies suggest developing a (relatively) simple model that is tractable Nano-Gels to Marine Snow: A Synthesis of Gel Formation Processes and related to the available data will enable us to step forward into new research by following and Modeling Efforts Involved with marine snow formation under different conditions. In this review, we synthesize the chemical and Particle Flux in the Ocean. Gels 2021, physical processes. We emphasize where these connections may lead to a predictive, mechanistic 7, 114. https://doi.org/10.3390/ understanding of the role of gels in marine snow formation and the biogeochemical functioning of gels7030114 the ocean. Academic Editor: Bjørn Torger Stokke Keywords: DOM; marine microgels; marine snow; polymer networks theory; biopolymer self- assembly; primary production; phytoplankton secretion; microbial loop; mathematical modeling Received: 11 July 2021 Accepted: 6 August 2021 Published: 9 August 2021 1. Introduction Publisher’s Note: MDPI stays neutral Global biogeochemical cycling of carbon, nitrogen, and other macro- and micro- with regard to jurisdictional claims in published maps and institutional affil- elements occurs throughout the water column of the oceans. A fraction of the photosyn- iations. thetically produced carbon in the sunlit photic zone is modified by biotic processes viz the microbial loop and the biological pump [1–7]. Up to 50% of the organic carbon produced by phytoplankton is thought to be taken up by bacteria, which are subsequently grazed by nanoplanktonic heterotrophic flagellates that drive the flux of material and energy into the food chain [3,6,8]. Bacteria, which solubilize particles and acquire dissolved organic carbon Copyright: © 2021 by the authors. (DOC) and inorganic nutrients, are then grazed upon by protozoa, and are subsequently Licensee MDPI, Basel, Switzerland. preyed on by mucus net-makers and small zooplankton, the latter of which function as con- This article is an open access article duits to higher trophic levels. In this way, the passively settling particles below the photic distributed under the terms and conditions of the Creative Commons zone, known as marine snow (Figure1), are regarded as a primary source of substrate that Attribution (CC BY) license (https:// supports heterotrophic food webs [9,10]. The vertical flux of carbon and nutrients relies on creativecommons.org/licenses/by/ sinking particles [11]. The flux of particulate organic carbon (POC) through sinking marine 4.0/). Gels 2021, 7, 114. https://doi.org/10.3390/gels7030114 https://www.mdpi.com/journal/gels Gels 2021, 7, x FOR PEER REVIEW 2 of 14 Gels 2021, 7, 114 2 of 14 nutrientssnow from relies surface on waterssinking declines particles exponentially [11]. The flux due of to particulate consumption, organic with onlycarbon 1% (POC) of the throughsinking organicsinking material marine reachingsnow from the surface seafloor waters [12]. declines exponentially due to con- sumption, with only 1% of the sinking organic material reaching the seafloor [12]. Figure 1. AA conceptual conceptual model model of of marine marine snow snow formation formation that that requir requireses the the following following steps: steps: (1) (1)microbial microbial cell cellgrowth; growth; (2) secretion of gels (i.e., biopolymers) aka polymeric substances from microbial cells; (3) formation of exopolymeric sub- (2) secretion of gels (i.e., biopolymers) aka polymeric substances from microbial cells; (3) formation of exopolymeric stances (EPS) which have a variety of forms including TEP and CSP; (4) reversible formation of nano-gels; (5) reversible substances (EPS) which have a variety of forms including TEP and CSP; (4) reversible formation of nano-gels; (5) reversible formation of micro-gels; (5) reversible or irreversible formation of macro-gels; (6) apparent stickiness of particle population dependentformation of on micro-gels; their protein (5) content, reversible i.e., or their irreversible protein-to-carbohy formation ofdrate macro-gels; (P/C) ratio; (6) apparent (7) irreversib stickinessle chemical of particle crosslinking population of proteinsdependent in gels on their to form protein marine content, snow i.e.,through their hydrophobic protein-to-carbohydrate or reactive oxygen (P/C) ratio;species (7) (ROS) irreversible mediated chemical chemical crosslinking crosslink- ing;of proteins (8) UV inoxidation; gels to form(9) interactions marine snow of mineral through surfaces hydrophobic with gels or reactiveor marine oxygen snow; speciesand (10) (ROS) aggregation-disaggrega- mediated chemical tion/fragmentationcrosslinking; (8) UV rates. oxidation; Nanogels (9) (100–150 interactions nm) of< microgels mineral surfaces (~5 µm) with< macrogel gels ors (100 marine µm) snow; < marine and snow (10) aggregation-(>500 µm to 10sdisaggregation/fragmentation of cm) occur on a size continuum. rates. Nanogels (100–150 nm) < microgels (~5 µm) < macrogels (100 µm) < marine snow (>500 µm to 10s of cm) occur on a size continuum. There is a complicated relationship between DOC and POC, with studies showing a dynamicThere equilibrium is a complicated between relationship free and assembled between DOCDOC andoccurring POC, withover studiesthe whole showing water columna dynamic that equilibrium produces micron-scale between free gel and patchiness assembled that DOC may occurringhelp to explain over thecarbon whole turno- wa- ver,ter columnparticularly that in produces the dark micron-scale ocean [13,14]. gel In patchiness addition, Arrieta that may et al. help [15] to found explain that carbon DOC isturnover, as readily particularly consumed in by the bacteria dark ocean in the [13 su,14rface]. In addition,as in the deep Arrieta ocean; et al. with [15] foundrates con- that strainedDOC is asonly readily by the consumed availability by of bacteria these materials. in the surface A generic as in relationship the deep ocean; between with DOC rates andconstrained organic onlybiopolymers by the availability forming ofexopolymeric these materials. substances A generic (EPS) relationship [16,17] or between transparent DOC exopolymericand organic biopolymers particles (TEP) forming [5,18–20] exopolymeric and larger substances marine snow (EPS) composites [16,17] or transparent[21–23] has beenexopolymeric suggested particles [24] but not (TEP) yet [objectiv5,18–20]ely and verified. larger The marine goal snow of this composites review is to [ 21synthesize–23] has historicalbeen suggested and recent [24] but literature not yet to objectively examine verified.the relationship The goal (if of one this exists) review between is to synthesize biopol- ymershistorical released and recent by microbes literature and to marine examine snow the relationship(Figure 1). This (if one is one exists) of the between major biopoly-gaps in ourmers understanding released by microbes of the mechanisms and marine that snow lead (Figure to marine1). This snow is formation one of the and major our gaps ability in toour accurately understanding model of particle the mechanisms processes that and lead fluxes to marine in the snowocean. formation Recent studies and our suggest ability Gels 2021, 7, 114 3 of 14 to accurately model particle processes and fluxes in the ocean. Recent studies suggest developing a (relatively) simple model that is tractable and related to the available data; this will enable us to step forward into new research by following marine snow formation under different conditions. This is critical given the variety of anthropogenic factors that are modifying biogeochemical cycles in the marine environment, specifically those whose fate and transport is intrinsically linked to marine snow formation. This includes but is not limited to engineered nanoparticles (e.g., [25,26]), oil spills and dispersants (e.g., [27–30]), and nano- and micro-plastics